The avian subpallium: New insights into structural and functional subdivisions occupying the lateral subpallial wall and their embryological origins

Abstract

The subpallial region of the avian telencephalon contains neural systems whose functions are critical to the survival of individual vertebrates and their species. The subpallial neural structures can be grouped into five major functional systems, namely the dorsal somatomotor basal ganglia; ventral viscerolimbic basal ganglia; subpallial extended amygdala including the central and medial extended amygdala and bed nuclei of the stria terminalis; basal telencephalic cholinergic and non-cholinergic corticopetal systems; and septum. The paper provides an overview of the major developmental, neuroanatomical and functional characteristics of the first four of these neural systems, all of which belong to the lateral telencephalic wall. The review particularly focuses on new findings that have emerged since the identity, extent and terminology for the regions were considered by the Avian Brain Nomenclature Forum. New terminology is introduced as appropriate based on the new findings. The paper also addresses regional similarities and differences between birds and mammals, and notes areas where gaps in knowledge occur for birds.

Full text

Review
The avian subpallium: New insights into structural and
functional subdivisions occupying the lateral subpallial wall
and their embryological origins
Wayne J. Kuenzel
a,
⁎, Loreta Medina
b
, Andras Csillag
c
, David J. Perkel
d
, Anton Reiner
e
a
Department of Poultry Science, Poultry Science Center, University of Arkansas, Fayetteville, Arkansas 72701, USA
b
Department of Experimental Medicine, Universitat de Lleida, Institute of Biomedical Research of Lleida (IRBLLEIDA), 25008 Lleida, Spain
c
Department of Anatomy, Histology and Embryology, Semmelweis University, Faculty of Medicine, H-1094, Budapest, Hungary
BRAIN RESEARCH 1424 (2011) 67–101
⁎Corresponding author. Fax: +1 479 575 7139.
E-mail address: wkuenzel@uark.edu (W.J. Kuenzel).
Abbreviations: 6-OHDA, 6-hydroxydopamine; A, Arcopallium; A6, Locus coeruleus, noradrenergic cell group; A8, Dopaminergic cell group;
Ac, AcS, AcC, Nucleus accumbens (shell and core); AChE, Acetylcholine esterase; AEP,Anterior peduncular area; AFP, Anterior forebrain path-
way; AHi, Amygdalo-hippocampal area; AMPA, Glutamate agonist specific for AMPA-gated glutamate receptor subtype; APH, Parahippocam-
pal area; ARCO, Arcopallium; Av, Arcopallium ventrale; AVT, Arginine vasotocin; BDA, biotinylated dextran amine; BG, dBG, vBG, Basal
ganglia, dorsal, ventral BG; BO, Bulbus olfactorius, olfactory bulb; BST, BSTL, BSTLdl,vm, Bed nucleus of the stria terminalis, lateral BST(BSTL),
BSTL pars dorsolateralis (BSTLdl), BSTL pars ventromedialis (BSTLvm); BSTM1, BSTM2, Medial BST sub-nucleus 1(dorsolateralis, dl), sub-nucleus
2(ventromedialis, vm); CA, Commissura anterior, anterior commissure; CCS, Caudocentral septal area; CeA, Central amygdalar nucleus; CGRP,
Calcitonin gene-related peptide; ChAT, Choline acetyltransferase; CHCS (FiHp), Tractus cortico-habenularis and tractus cortico-septalis (fimbria
of hippocampus); CLSt, Caudolateral part of striatum; CoS, Nucleus commissuralis septi, commissural septal nucleus; CPa (HpC), Pallial commis-
sure (hippocampal commissure); CPu, Caudate putamen; CRH, Corticotropin releasing hormone; CSFcn, Cerebrospinal fluid contacting neuron/
s;cSP,SP,ChickensubstanceP;CVO,Circumventricularorgan/s;DA,Dopamine; DARPP, Dopamine and cAMP-regulated phosphoprotein; DIEN,
Diencephalon; DL CPu, Dorsolateral part of caudate putamen; DLM, Medial dorsolateral nucleus of the anterior thalamus; DMA, Anterior dor-
somedial thalamic nucleus; DVR, Dorsal ventricular ridge; DYN, Dynorphin; E14, E16, E18, Embryonic day 14, 16 and 18 in developing chick;
EA, Extended amygdala; EAce, cel, cem, Central EA, lateral part of EAce (EAcel), medial part of EAce (EAcem); EAmes, Medial EA, subpallial part;
EAp, Pallial part of the medial EA; ENK, Enkephalin; GABA, Gamma-aminobutyric acid; GAD, Glutamic acid decarboxylase; GnRH-1, Gonadotro-
pin releasing hormone-1; GP, GPe, GPi, Globus pallidus, GP externus (GP e), GP internus (GPi); H, Hyperpallium (dorsal pallium); HVC, HVC, used as
a letter based name (associative center of the caudal nidopallium); IHA, Interstitial nucleus of the apical hyperpallium; INP, Intrapeduncular nu-
cleus; IP, Interpeduncular nucleus; ITC, Intercalated amygdalar cells; LAMP, Limbic-associated membrane protein; LFB, Lateral forebrain bundle;
LGE, Lateral ganglionic eminence; LMAN, Lateral magnocellular nucleus of the anterior nidopallium; LoC, Locus coeruleus (A6), noradrenergic
cell group; LPS, Pallial-subpallial lamina; LS, Lateral septum; LSO, LSOm, LSOl, Lateral septal organ, pars medialis (LSOm), pars lateralis (LSOl);
LSt, Lateral striatum; M, Mesopallium (lateral pallium); MeA, Medial amygdala; MeAs, Subpallial medial amygd ala; MFB, Medial forebrain bundle;
MGE, MGEcv, Medial ganglionic eminence, caudalventral area; MPTP, 1-methy-4-phenyl-1,2,3,6-tetrahydropyridine; MSIB, Medial septum, inter-
nal band; MSt, Medial striatum (MSt); MStm, Medial striatum, magnocellular part; N, Nidopallium; NBM, Nucleus basalis magnocellularis (of
Meynert), basal magnocellular n; NCPa (NHpC), Bed nucleus of pallial commissure, replaced by NHpC; NDB, NDBh,v, Nucleus of the diagonal
band, horizontal limb, ventricular limb; N-III, Third cranial nerve (oculomotor nerve); NHpC, Nucleus of hippocampal commissure; NMDA, Glu-
tamate agonist specific for NMDA-gated glutamatereceptorsubtype;NOS,Nitricoxidesynthase;NPY,NeuropeptideY;NTS,Nucleustractus
solitarius; OB, Olfactory bulb; OVLT, Organum vasculosum of the lamina terminalis; PO, Preoptic area; PoA, PoAc, Posterior nucleus of the pallial
amygdala,compactdivision;POC,Commissuralpreopticarea;PPN,Pedunculopontinenucleus;Pt,Pretectum;RSv,Ventralreticularsuperior
nucleus; S, Se, Septum; SL, Nucleus septalis lateralis, Lateral septal nucleus; SM, Nucleus septalis medialis, Medial septal nucleus; SNc, Substan-
tia nigra pars compacta; SNr,Substantianigra pars reticulata; SpA, Subpallial amygdaloid area; SpL, Lateral spiriform nucleus; SPV, Supraopto-
paraventricular domain; SS, Somatostatin; SSO, Subseptal organ; ST, Stria terminalis; StC, Striatal capsule; Std, Dorsal striatal subdivision;
STN, Subthalamic nucleus (formerly, anterior nucleus of the ansa lenticularis); Stvb, Stvi, Ventral striatal subdivision, basal domain, interme-
diate domain; Supv, Subparaventricular nucleus (part of suprachiasmatic domain of embryo); TEO, Optic tectum; Th, Thalamus; TH, Tyrosine
hydroxylase; TnA, Nucleus taeniae of the amygdala, currently proposed as the subpallial medial amygdala (MeAS); TPO, Area temporo-
parieto-occipitalis; TRH, Thyroid releasing hormone; TSM, Tractus septopallio-mesencephalicus; TuO, Olfactory tubercle; Tup, Tus, Pallidal
olfactory tubercle, striatal olfactory tubercle; vaf, Ventral amygdalofugal tract (formerly occipitomesencephalic tract); VIA, Ventrointermedi-
ate thalamic area; VL, Lateral ventricle; VP, VPa, Ventral pallidum; VTA, Ventral tegmental area
0006-8993/$ –see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.brainres.2011.09.037
Available online at www.sciencedirect.com
www.elsevier.com/locate/brainres

d
Departments of Biology and Otolaryngology, University of Washington, Seattle, Washington 98195-6515, USA
e
Departments of Anatomy and Neurobiology; and, Ophthalmology, University of Tennessee Health Science Center, Memphis,
Tennessee 38163, USA
ARTICLE INFO ABSTRACT
Article history:
Accepted 17 September 2011
Available online 24 September 2011
The subpallial region of the avian telencephalon contains neural systems whose
functions are critical to the survival of individual vertebrates and their species. The
subpallial neural structures can be grouped into five major functional systems, namely
the dorsal somatomotor basal ganglia; ventral viscerolimbic basal ganglia; subpallial
extended amygdala including the central and medial extended amygdala and bed nuclei
of the stria terminalis; basal telencephalic cholinergic and non-cholinergic corticopetal
systems; and septum. The paper provides an overview of the major developmental, neu-
roanatomical and functional characteristics of the first four of these neural systems, all of
which belong to the lateral telencephalic wall. The review particularly focuses on new
findings that have emerged since the identity, extent and terminology for the regions
were considered by the Avian Brain Nomenclature Forum. New terminology is introduced
as appropriate based on the new findings. The paper also addresses regional similarities
and differences between birds and mammals, and notes areas where gaps in knowledge
occur for birds.
© 2011 Elsevier B.V. All rights reserved.
Keywords:
Basal ganglia
Striatum
Pallidum
Basal forebrain
Extended amygdala
Corticopetal system
Contents
1. Introduction .......................................................... 69
2. Organization of the subpallium................................................ 70
2.1. Definition and components of the subpallium ................................... 70
2.2. Developmental origin ................................................. 70
3. Four neural systems occupying the lateral subpallial wall ................................. 75
3.1. Dorsal somatomotor basal ganglia .......................................... 75
3.1.1. Medial striatum ................................................ 75
3.1.2. Lateral striatum ................................................ 78
3.1.3. Intrapeduncular nucleus ........................................... 78
3.1.4. Globus pallidus................................................. 79
3.1.5. Functional considerations for dorsal basal ganglia . . . .......................... 79
3.1.6. Area X: A specialized songbird striatal structure. .............................. 81
3.2. Ventral viscerolimbic basal ganglia.......................................... 82
3.2.1. Olfactory tubercle ............................................... 82
3.2.2. Nucleus accumbens core and shell ...................................... 83
3.2.3. Ventral pallidum................................................ 85
3.2.4. Functional considerations for ventral basal ganglia . . . .......................... 85
3.3. Subpallial amygdaloid nuclei: The extended amygdala —central and medial amygdala, and bed nuclei
of the stria terminalis ................................................. 86
3.3.1. Central extended amygdala and BSTL .................................... 86
3.3.2. Functional considerations for the central extended amygdala complex .................. 88
3.3.3. Medial extended amygdala and BSTM .................................... 89
3.3.4. Functional considerations for subpallial medial amygdala and BSTM ................... 90
3.4. Basal telencephalic cholinergic and non-cholinergic corticopetal system ..................... 90
3.4.1. Nucleus basalis magnocellularis ....................................... 91
3.4.2. Nucleus of the diagonal band ......................................... 91
3.4.3. Nucleus commissuralis septi (Commissural septal nucleus) ........................ 92
3.4.4. Functional considerations for corticopetal system . . . .......................... 92
4. Conclusions .......................................................... 92
Acknowledgments ......................................................... 92
References.............................................................. 92
68 BRAIN RESEARCH 1424 (2011) 67–101

1. Introduction
A revised terminology of the avian forebrain was proposed in
2004 (Reiner et al., 2004b) as a result of an international Nomen-
clature Forum held at Duke University in July of 2002. The revi-
sion became necessary due to the longstanding existence of an
inappropriate terminology for many forebrain structures based
upon persistent but outdated and erroneous assumptions of
homology to mammalian brain structures (Jarvis et al., 2005;
Reiner, 2005; Reineret al., 2004b). Historically, a single structure,
the basal ganglia, was thought to comprise most of the fore-
brain of birds (Edinger, 1908; Elliot-Smith, 1901; Herrick, 1956).
Forty years ago, a seminal hypothesis was put forth by Harvey
Extended amygdala and BST
Central extended amygdala (SpA,BSTL)
Medial extended amygdala (MeAs,BSTM1,BSTM2)
Ventral viscerolimbic BG(TuO,AcS,AcC,VP)
Dorsal somatomotor BG(MSt,LSt,INP,GP)
NEURALSYSTEMSINTHESUBPALLIUM
Basal telencephalic corticopetal system
(NBM,NDB,CoS)
Septum and septal neuroendocrine system
(SM,SL,NHpC,LSO,OVLT,SSO)
LPS
ARCO
DIEN
Fig. 1 –Schematic diagram of five neural systems comprising the avian subpallium.
Red Dorsal somatomotor basal ganglia: structures include the lateral striatum (LSt), medial striatum (MSt), globus pallidus (GP),
intrapeduncular nucleus (INP) and pallial–subpallial lamina (LPS; the dorsal border of LSt and MSt).
Tan Ventral viscerolimbic basal ganglia: structures include the olfactory tubercle (TuO), nucleus accumbens (shell and core, AcS, AcC) and
ventral pallidum (VP).
Blue Extended amygdala and bed nuclei of the stria terminalis: structures include the central extended amygdala–subpallial amygdaloid area (SpA),
striatal capsule (StC) and lateral bed nucleus of the stria terminalis (BSTL); and, the medial extended amygdala–subpallial medial
amygdala (MeAs) and medial bed nucleus of the stria terminalis (BSTM1, BSTM2).
Green Basal telencephalic cholinergic and non-cholinergic corticopetal system: structures include the basal magnocellular nucleus (NBM), diagonal
band nucleus (NDB) and commissural septum (CoS).
Yellow Septum and septal neuroendocrine systems: structures include the medial Septum (SM), lateral septum (SL), nucleus of the hippocampal
commissure (NHpC) and circumventricular organs —lateral septal organ (LSO), organum vasculosum of the lamina terminalis (OVLT)
and subseptal organ (SSO).
Other abbreviations: ARCO —arcopallium, DIEN —diencephalon.
69BRAIN RESEARCH 1424 (2011) 67–101

Karten that the basal ganglia occupied a much more restricted
basal region of the avian telencephalic hemispheres (Karten,
1969; Nauta and Karten, 1970). Numerous subsequent studies
confirmed this hypothesis, and more broadly showed that the
entire basal telencephalon (the subpallium) in birds contained
homologues of many cell groups found in the subpallial telen-
cephalon in mammals. One of the major goals of the Nomencla-
ture Forum was to rename regions of the telencephalon in birds
with terms that accurately reflect the new understanding
of their homology to mammalian telencephalic regions.
This resulted in the re-naming of nearly all structures in the
two major regions (i.e. the pallium and subpallium) of the
avian telencephalon. Since the time of the Forum, new ana-
tomical, electrophysiological, embryological, behavioral and
gene expression data have accrued on the organization and
development of the somatic basal ganglia in birds, as well
as the visceral basal ganglia, subpallial amygdala, basal fore-
brain cholinergic system, and septum. The new findings ex-
tend the understanding of these regions, especially with
respect to their function and mammalian homologues. The
present review seeks to provide an updated synthesis of the
avian subpallium, focusing on the lateral subpallial wall.
2. Organization of the subpallium
2.1. Definition and components of the subpallium
The subpallium in birds consists of telencephalic structures
ventral to the pallial–subpallial lamina (LPS), medial to the
arcopallium/pallial amygdala, and rostro-dorsal to the dien-
cephalon (Fig. 1). Subpallial structures can be organized into
five major groups (Table 1), based on developmental, topo-
graphic, neurochemical, hodological and functional criteria.
Four groups are located lateral to the ventral horns of the lat-
eral ventricles, while the fifth group resides medial to the ven-
tral horns of the lateral ventricles thereby occupying the
medial wall of subpallium (Fig. 1). The five groups and their
constituent major structures are:
1) Dorsal Somatomotor Basal Ganglia, consisting of the later-
al striatum, dorsal part of medial striatum, the globus pal-
lidus, and the intrapeduncular nucleus.
2) Ventral Viscerolimbic Basal Ganglia, consisting of the ol-
factory tubercle, ventral part of medial striatum, nucleus
accumbens, and ventral pallidum.
3) Extended Amygdala, consisting of two components: (1) central
extended amygdala which includes the so-called subpallial
amygdala, an apparent central amygdala homologue, and
the lateral bed nucleus of the stria terminalis, and, (2) the me-
dial extended amygdala comprising the subpallial medial
amygdala homologue (i.e. the subpallial nucleus taeniae) and
the medial bed nucleus of the stria terminalis.
4) Basal Telencephalic Cholinergic and Non-cholinergic Cor-
ticopetal System, consisting of: the nucleus basalis magno-
cellularis, the nucleus of the diagonal band, and nucleus
commissuralis septi.
5) Septum and Septal Neuroendocrine Systems, consisting of:
the medial septum, the lateral septum, the nucleus of the
hippocampal commissure (previously known as the bed
nucleus of the pallial commissure), the lateral septal
organ, the organum vasculosum of the lamina terminalis,
and the subseptal organ.
Of these five systems, the first four residing withinthe later-
al wall of subpallium will be reviewed here because of the close
associations with intratelencephalic circuitry, motor function,
and reward-motivated learning. The Septum and Septal Neuro-
endocrine System occurring medially between the ventral
horns of the lateral ventricles and more closely associated
with downstream diencephalon neuroendocrine functions
and related social behaviors, will be reviewed in a later paper.
2.2. Developmental origin
The subpallium in both birds and mammals forms in the basal
telencephalic anlage during development, and gives rise to the
structures of the mature basal telencephalon, which are thus re-
ferred to as subpallial structures (Cobos et al., 2001b; Holmgren,
1925; Källén, 1951, 1953, 1962; Marín and Rubenstein, 2001;
Table 1 –Structures comprising the subpallium.
Structures within the lateral wall of subpallium
1. Somatic basal ganglia
a. Somatic striatum (striatal region)
i. Dorsal and ventral parts of medial striatum
ii. Lateral striatum
iii. Nucleus intrapeduncularis
iv. Area X (mixed striatal and pallidal region)
b. Globus pallidus (GP; pallidal region)
2. Limbic basal ganglia
a. Limbic striatum (striatal region)
i. Ventral part of medial striatum
ii. Nucleus accumbens shell and core
iii. Olfactory tubercle —rostral and dorsolateral
b. Limbic pallidum (pallidal region)
i. Ventral pallidum
ii. Olfactory tubercle —posterior and caudomedial
3. Extended amygdala complex
a. Extended central amygdala complex (mixed striatal and
pallidal region)
i. Subpallial amygdaloid area
ii. Lateral bed nucleus of stria terminalis
b. Extended medial amygdala complex (pallidal region)
i. Nucleus taeniae amygdala (subpallial medial amygdala)
ii. Medial bed nucleus of stria terminalis
4. Cholinergic corticopetal system (commissural preoptic areal
derivatives)
a. Nucleus basalis magnocellularis
b. Nucleus of the diagonal band (mixed commissural preoptic
area and pallidal region)
c. Nucleus of the septal commissure
Structures within the medial wall of subpallium
1. Septum and septal neuroendocrine system
a. Medial septum
b. Lateral septum
c. Nucleus of hippocampal commissure (formerly termed the
bed nucleus of pallial commissure)
d. Circumventricular organs: (lateral septal organ, organum
vasculosum of the lamina terminalis and subseptal organ)
70 BRAIN RESEARCH 1424 (2011) 67–101

Pombero and Martínez, 2009; Puelles et al., 2000; Striedter,
1997). Current gene expression and fate mapping data indicate
that the subpallium possesses three major radially-oriented his-
togenetic zones (Fig. 2) during development: 1) a dorsal, striatal
zone termed the lateral ganglionic eminence (LGE) in mammals,
which produces striatal subdivisions of the dorsal and ventral
basal ganglia and the subpallial amygdala; 2) a ventral, pallidal
subdivision called the medial ganglionic eminence (MGE) in
mammals, which produces pallidal subdivisions of the dorsal
and ventral basal ganglia and the subpallial amygdala; and
3) the preoptic subdivision (POC) in the telencephalic stalk,
which contributes to the subpallial amygdala, and gives rise
to most of the cholinergic cells of the basal forebrain cortico-
petal system (Abellán and Medina, 2008, 2009; Cobos et al.,
2001a,b; Flames et al., 2007; García-López et al., 2008; Marín
and Rubenstein, 2001; Puelles et al., 2000, 2007; Redies et al.,
2001). Recent data in the chicken and mouse indicate that
each of these three zones is divided into further subzones,
each giving rise to different parts of the striatum, pallidum
and subpallial amygdala, as detailed below.
The entire subpallium in birds and mammals is defined by
expression of the transcription factors Dlx2/5 and the neuro-
genetic gene Mash1 (or its ortholog in other vertebrates).
These are involved in regulating the production of GABAergic
neurons, which are the predominant and defining neuron
type of the subpallium (Abellán and Medina, 2009; Garda
et al., 2002; Puelles et al., 2000; Wullimann and Mueller,
2004). By contrast, the predominant and defining neuron
type of the pallium is glutamatergic (Abellán et al., 2009).
The striatal subdivision of the developing subpallium is dis-
tinct from the pallidal and preoptic zones in that it expresses
Gsh2,Pax6 and the LIM-only gene Lmo4, in addition to Dlx2/5
and Mash1. This is particularly evident using coronal sections
of embryonic chick(c) hybridized for cLmo4 (Figs. 3C–F) and c
substance P (cSP) (Figs. 3A–B) which mark major striatal compo-
nents of the dorsal somatomotor and ventral viscerolimbic
basal ganglia. By contrast, the pallidal and the preoptic
zones additionally express the transcription factors Nkx2.1,
Lhx6 and Lhx7/8, with the preoptic subdivision also showing
strong ventricular expression of Sonic hedgehog (Abellán and
Fig. 2 –Schematic diagram of the three major, developmental subpallial proliferative zones and their derivatives, comparing
mouse and chicken. The three major subpallial divisions are: lateral ganglionic eminence (LGE) in mouse, and the corresponding
striatal division (St) in chicken; medial ganglionic eminence (MGE) in mouse, and the corresponding pallidal division (Pa) in
chicken; and the preoptic division (PO) in mouse and commissural preoptic division (POC) in chicken. Based on differential gene
expression patterns (for example, differential expression of the transcription factors Pax6, Islet1 or Nkx2.1), each major division is
subdivided into several subdomains, although some differences are found in the number of subdivisions between mouse and
chicken. For example, four LGE subdivisions are found in mouse, but only three striatal subdivisions appear to be present in
chicken: 1) dorsal striatal (dorsal st.), 2) ventrointermediate striatal (ventroint. st.) and 3) ventrobasal striatal (ventrobas. st.)
subdivisions which may be related to some of the differences found in the mature striatum of these two species. Similarly,
although five MGE subdivisions are present in mouse, only three have been described in chicken: 1) dorsal pallidal (dorsal pa.),
2) ventral pallidal (ventral pa.) and 3) caudal pallidal (formerly termed the anterior peduncular area (AEP)) subdivisions. Regarding
the preoptic area, two comparable subdivisions are found in mouse and chicken, although here we only refer to one of them
(the commissural preoptic subdivision or POC) due to its contribution of cells to the lateral telencephalic wall. See text for more
details and list of abbreviations for other abbreviations shown in figure.
71BRAIN RESEARCH 1424 (2011) 67–101

Medina 2009; Flames et al., 2007; García-López et al., 2008;
Garda et al., 2002; Puelles et al., 2000). Thus, each of the
three major subpallial histogenetic zones (striatal, pallidal
and preoptic) expresses a unique and defining combination
of genes that are thought to control development of those re-
gions. Note that the so-called caudal ganglionic eminence of
mammals, previously proposed to represent a separate sub-
pallial subdivision (Nery et al., 2002), is now thought to repre-
sent the caudal parts of both the lateral and medial ganglionic
eminences (Flames et al., 2007; García-López et al., 2008).
Studies in mice and other neurogenetic models have begun
to clarify the role of these genes and their hierarchical interac-
tions during development. Gsh1/2 and Nkx2.1 are among the
earliest transcription factors expressed in the mouse subpal-
lium, and they play key roles in patterning and specification
of the striatal and pallidal subdivisions, respectively (Sussel
et al., 1999; Yun et al., 2001, 2003). The role of Gsh1/2 in striatal
formation is evidenced by the absence or malformation of the
striatum in Gsh2-null mice (Yun et al., 2001)orGsh1/2-double
null mice (Yun et al., 2003). Similarly, the role of Nkx2.1 in pal-
lidal development is evidenced by the severe pallidal malfor-
mation in Nkx2.1-null mice (Sussel et al., 1999). Gsh1/2 and
Nkx2.1 are transcription factors that regulate the expression
of downstream transcription factors, such as Mash1,Dlx1/2,
Lhx6, and Lhx7/8 (Sussel et al., 1999; Toresson et al., 2000;
Yun et al., 2001, 2003). Mash1 and Dlx1/2 have been shown by
studies in mice to be involved in the neurogenesis and differ-
entiation of subpallial GABAergic neurons (Cobos et al., 2005;
Long et al., 2009a,b; Stühmer et al., 2002a,b), while Lhx7/8
plays a key role in the differentiation of cholinergic neurons
(Zhao et al., 2003). Most of these transcription factors are
expressed in chicken subpallium in patterns identical to
those in mouse (e.g., Dlx2/5,Nkx2.1,Lhx6,Lhx7/8). While it
seems likely their function is similar, this has not been direct-
ly demonstrated. Nonetheless, the correlated expression of
Dlx2/5 and GAD67 (a synthetic enzyme for GABA) in chicken
and Xenopus suggests that Dlx transcription factors play a
role in differentiation of GABAergic neurons in the forebrain
of nonmammalian vertebrates as well (Abellán and Medina,
2009; Brox et al., 2003). In addition, the correlated expression
of Lhx7/8 and ChAT (the synthetic enzyme for acetylcholine)
in chicken suggests that Lhx7/8 plays a role in the differentia-
tion of telencephalic cholinergic neurons in birds, much like it
does in mammals (Abellán and Medina, 2009). Moreover,
Nkx2.1-knockdown in Xenopus suggests that this transcription
factor also plays an evolutionarily conserved role in pallidal
specification and in the regulation of Lhx7/8 expression (van
der Akker et al., 2008).
The striatal and pallidal zones possess subdomains that are
characterized by expression of distinct combinations of devel-
opmental regulatory genes, with each giving rise to specificsub-
populations of subpallial neurons (Abellán and Medina, 2009;
Flames et al., 2007). In chicken, the developing striatal progeni-
tor zone includes three subdivisions. Early in development
there are only two, a dorsal and ventral, with the ventral then
later subdividing into separate ventrointermediate and ventro-
basal zones to make three distinct striatal progenitor regions.
These three striatal subdomains have been identified in
mouse as well, and mice additionally possess a fourth zone,
not evident in birds, interposed between the initial dorsal and
ventral subdomains. In both chickens and mice, the two ventral
subdivisions are the source of the bulk of the dorsal and ventral
striatum. The dorsal subdivision is characterized by expression
of the transcription factor Pax6 in both mitotic and postmitotic
cells, and the ventral subdivision expresses the transcription
factor Islet1 in the subventricular zone and mantle (Abellán
and Medina, 2009; Puelles et al., 2000; Stenman et al., 2003;
Yun et al., 2001). Based on the expression of Pax6 and correlation
with data on mammals, the dorsal striatal subdivision also
appears to be the source of GABAergic and dopaminergic in-
terneurons that migrate into the olfactory bulb (Abellán and
Medina, 2009). The dorsal striatal subdivisions may thus
also be the source of catecholaminergic–dopaminergic neurons
in the olfactory tubercle of some birds (Abellán and Medina,
2009; Roberts et al., 2002), and in the striatum of mice and pri-
mates (Huot and Parent, 2007; Marín et al., 2005). The dorsal
striatal subdomain also produces part of the lateral striatum
in chicken (Abellán and Medina, 2009), and similarly in mouse
Fig. 3 –A–F present low-magnification digital images of frontal
sections of the telencephalon of chicken at prehatching stages
(E18) or at hatching (P0), hybridized for cSP (A, B), cLmo4 (C–F).
The images show the major subdivisions of the developing
somatic and limbic basal ganglia, with striatal subdivisions
enriched in cSP and cLmo4. Scale bar=1 mm in A (applies to A,
B), and Scalebar=1 mm in C (applies to C–F). AcC = accumbens
core; AcS = accumbens shell; StC = striatal capsule; Tup =
pallidal olfactory tubercle; Tus = striatal olfactory tubercle.
From Abellán and Medina (2009). See list of abbreviations for
other abbreviations shown in this figure.
72 BRAIN RESEARCH 1424 (2011) 67–101

some neurons of the dorsolateral striatum (Toresson and
Campbell, 2001; Yun et al., 2003). At caudal hemispheric levels
in both chicken and mouse, this dorsal striatal subdivision
also appears to produce Pax6-expressing striatal neurons for
the central amygdala in both chicken and mouse (Abellán and
Medina, 2009; Puelles et al., 2000; Tole et al., 2005). Finally, a
thin group of neurons directly below the palliosubpallial lamina
also appears to be part of the dorsal striatal subdivision. This re-
gion distinctly expresses Lmo4 (Abellán and Medina, 2009)and
the Enc1 gene (ectodermal and neural crest cortex), a homolog
of Kelch aDrosophila melanogaster gene essential for oogenesis
(García-Calero and Puelles, 2009; Puelles et al., 2007), and it
overlaps the subpallial area expressing Pax6. Since intercalated
cell masses of the mammalian amygdala derive from the dorsal
LGE based on gene expression and fatemap data (Kaoru et al.,
2010; Tole et al., 2005; Waclaw et al., 2010), the Lmo4-expressing
striatal capsular region in chicken has been proposed to be ho-
mologous to the amygdaloid intercalated cell masses of mam-
mals (Abellán and Medina, 2009).
Based on genetic fate mappingof Islet1 progenitors in mouse,
most neurons of the striatal part of the basal ganglia (including
the majority of projection neurons of dorsal and ventral stria-
tum) derive from the two parts of the ventral striatal subdivi-
sion or ventral LGE (Stenman et al., 2003; Waclaw et al., 2010;
reviewed in Medina and Abellán, 2009), and this appears to be
true in chicken as well (Abellán and Medina, 2009). In contrast,
most striatal interneurons in mouse and chicken derive from
the pallidal or preoptic subpallial progenitor zones (Abellán
and Medina, 2009; Cobos et al., 2001a; Marín et al., 2000;see
below). The striatal part of the developing basal ganglia in
birds, however, differs from that in mammals in the number
of regions making up the striatal progenitor zone. As noted
above, this region of the developing subpallium in birds comes
to consist of separate dorsal, ventrointermediate and ventroba-
sal subdomains, while inmammals an additional zone isinter-
posed between the dorsal and two ventral striatal zones.
This additional zone may giverise to the striosomal dorsal stria-
tal compartment in mammals, which may explain why this
compartment seems absent in birds (Abellán and Medina,
2009; Flames et al., 2007). The ventrointermediate striatal-
equivalent in mammals (LGE3 in mouse) then gives rise to the
projection neurons of the matrix compartment of dorsal stria-
tum, and in birds to the dorsal medial striatum and lateral stri-
atum. The ventrobasal striatal zone (corresponding to LGE4 in
mouse), in turn, gives rise to nucleus accumbens in birds and
mammals (Abellán and Medina, 2009). The ventrobasal zone
also appears to produce the INP in birds (Abellán and Medina,
2009).
The pallidal progenitor zone of mouse and chicken also
has molecularly distinct subdivisions (Abellán and Medina,
2009; Flames et al., 2007; García-López et al., 2008). Again, the
development of the pallidal subpallial regions is more com-
plex in mouse than in chicken, with mouse having five dis-
tinct progenitor subdomains and birds only three evident
ones (Abellán and Medina, 2009; Flames et al., 2007), although
one of the avian pallidal progenitor subdomains appears to
correspond to two MGE zones. Of those in mammals, the dor-
salmost seems absent in birds, and the second and third MGE
zones give rise to most neurons of the globus pallidus, and
correspond to the dorsal pallidal zone of chick, which also
gives rise to globus pallidus. As will be discussed below,
these various pallidal zones also contribute to the bed nucleus
of the stria terminalis and extended amygdala. In addition, re-
cent data indicate that the adult mouse globus pallidus in-
cludes a neuron subpopulation that originates in the striatal
progenitor zone (Nóbrega-Pereira et al., 2010). The neurons of
this subpopulation of the globus pallidus do not contain par-
valbumin, although they are GABAergic (Nóbrega-Pereira et
al., 2010), and likely represents a striatal-type subpopulation
of projection neurons that contain calbindin and enkephalin,
and project back to the striatum (Hoover and Marshall, 2002;
Medina and Abellán, 2009). A similar neuron subpopulation
also appears to be present in the chicken globus pallidus
(Abellán and Medina, 2009; Molnaret al., 1994). The mammalian
ventral pallidum possesses a rostral, precommissural part that
arises from MGE4, and a commissural ventral pallidum that
arises from MGE2/3 (Abellán and Medina, 2009; García-López
et al., 2008). The avian ventral pallidum, however, appears to
arise only from the MGE4-equivalent (i.e. the ventral pallidal
zone), and is thus homologous only to the precommissural ven-
tral pallidum (Abellán and Medina, 2009; García-López et al.,
2008). Both mouse and chicken possess a caudoventral pallidal
subdivision (MGEcv), which is included as a caudal part of the
fifth progenitor subdomain of the medial ganglionic eminence
(pMGE5; Flames et al., 2007), and is sometimes called the anteri-
or peduncular area (AEP) (Abellán and Medina, 2009; García-
López et al., 2008), that appears to giverise to part of themedial
extended amygdala, as discussed in more detail in a later
section.
Based on Sonic hedgehog (Shh) expression, the commissural
preoptic area (POC) of both mouse and chicken also appears to
contribute cells to the subpallial medial amygdala and other
parts of the medial extended amygdala, and this has been
shown experimentally in the mouse (Bupesh et al., 2011a).
Pallidal (MGEcv) and POC cells intermingle in the subpallial
medial amygdala of chicken, resembling in this respect the
anterior part of the medial amygdala of mammals (Abellán
and Medina, 2009; García-López et al., 2008). Recent data indi-
cate that the Lhx7/8 transcription factor is particularly highly
expressed in the POC of mouse and chicken (including the
ventricular zone where most progenitor cells are located)
and that this subdivision may be the source of many cholin-
ergic cells of the basal forebrain, including the corticopetal
neurons of the basal magnocellular nucleus (NBM) and
those overlapping the pallidum, as well as most of the cholin-
ergic interneurons of the striatum (Abellán and Medina, 2008;
2009; García-López et al., 2008). Data in mouse indicate that
Lhx8 (also called Lhx7/8)isrequiredfordevelopmentofmost
cholinergic neurons of the telencephalon, since they are
missing in Lhx7/8 knockout mouse (Manabe et al., 2007;
Zhao et al., 2003). The influence of Lhx7/8 is partially mediat-
ed by the transcription factor Islet1, which is expressed in sub-
ventricular and postmitotic cells of POC. This interpretation is
consistent since POC-derived cholinergic neurons of basal fore-
brain, pallidum and striatum are absent in conditional
forebrain-specific Islet1-null mouse (Elshatory and Gan, 2008).
Because most cholinergic neuronsof the medial septum/diago-
nal band nuclei are preserved in conditional Islet1-null mice
(Elshatory and Gan, 2008), these may derive from the rostroven-
tral MGE, a subdomain that expresses Lhx7/8 in its ventricular
73BRAIN RESEARCH 1424 (2011) 67–101

and subventricular zones, but not Islet1, in mouse and chicken
(Abellán and Medina, 2009; Flames et al., 2007; reviewed in Me-
dina and Abellán, 2009).
In summary, developmental and anatomical data suggest
the following categorization of lateral subpallial structures
(Table 1). Striatal regions derived from the striatal progenitor
zone are the lateral and medial striatum, accumbens core and
shell, intrapeduncular nucleus, part of the central extended
amygdala, and part of the olfactory tubercle. The pallidal regions
derived from the pallidal progenitor zone are the globus palli-
dus, ventral pallidum, part of the central and medial extended
amygdala, and some neuron subpopulations of the diagonal
band nuclei. The POC derivatives of the lateral subpallial wall
are the basal magnocellular nucleus, the cholinergic neurons
Fig. 4 –A–D. A series of schematic line drawings of midtelencephalic transverse brain sections of pigeon and rat. A. The
outdated interpretation of the organization of the telencephalon in birds and the outdated nomenclature that view engendered
for the telencephalon of birds. B. The longstanding interpretation of mammalian telencephalic organization and the
established nomenclature consistent with that view. C. The current interpretation of the organization of avian telencephalon
and the outdated avian telencephalic nomenclature, which highlights the inappropriateness of this nomenclature. D. The
current interpretation of the organization of avian telencephalon and new avian telencephalic nomenclature adopted by the
Avian BrainNomenclature Forum that is consistent with current findings on telencephalicorganization in birds. In each schematic
interpretation of telencephalic organization, the speckled region represents pallium, the striped region represents striatum, and
the checked region represents globus pallidus. The new avian terminology (D) avoids the erroneous misimpressions about
correspondences between avian and mammalian telencephala perpetuated by the old nomenclature. Hp = hippocampus.
From Reiner et al. (2004a, 2004b).
74 BRAIN RESEARCH 1424 (2011) 67–101

invading the pallidum and striatum, and part of the medial ex-
tended amygdala (Abellán and Medina, 2008, 2009; García-López
et al., 2008; Marín and Rubenstein, 2001). Although cells of each
subpallial nucleus/area primarily derive and primarily migrate
radially from a specific striatal, pallidal or preoptic subdivision,
there are important migrations that cross subdivision bound-
aries within the subpallium, or cell immigration from outside
the subpallium, leading to a mixed cellular composition in
most subpallial areas (Abellán and Medina, 2009; Cobos et al.,
2001a,b). This is the case for some components of the extended
amygdala, as will be discussed in more detail below. A strik-
ing case of tangential cell movement inside the avian subpal-
lium is the massive migration of cells from the pallidal
proliferative zone into the medial striatum demonstrated in
chickens (Abellán and Medina, 2009). This will be discussed
in more detail in the sections on the striatal part of the
somatic basal ganglia and in the section on area X, a striatal
nucleus of songbirds that contains both striatal and pallidal
neurons (Farries and Perkel, 2002; Person et al., 2008; Reiner
et al., 2004a). Finally, in both chicken and mouse, the subpal-
lium is the source of tangential migrations to the pallium,
providing it with various neurochemically distinct subpopu-
lations of GABAergic interneurons (Abellán and Medina,
2009; Cobos et al., 2001a, b; Marín and Rubenstein, 2001,
2003). The subpallium also appears to produce some cholin-
ergic interneurons for the pallium (Abellán and Medina,
2009).
Hence, the developing vertebrate subpallium, at least in
tetrapods, appears to commonly possess the same three
major progenitor zones or their correspondents: striatal, palli-
dal and POC (Fig. 2). Markers useful in identifying progenitor
zones have likewise been shown to give rise to homologous
subpallial cell groups of the lateral telencephalic wall in
birds and mammals, as well as reptiles and amphibians
(Bachy et al., 2002; Brox et al., 2003; Fernández et al., 1998;
González et al., 2002a,b; Moreno et al., 2004, 2008a,b,c, 2009).
In the following sections, we review recent progress on the
dorsal basal ganglia, the ventral basal ganglia, the subpallial
amygdala/extended amygdala, and the basal forebrain corti-
copetal system of birds.
3. Four neural systems occupying the lateral
subpallial wall
3.1. Dorsal somatomotor basal ganglia
Discovery in the 1960s of the abundance of dopamine and ace-
tylcholinesterase in the avian subpallium began to reshape
understanding of the location and extent of the avian basal
ganglia (Juorio and Vogt, 1967; Karten, 1969; Nauta and Karten,
1970; Spooner and Winters, 1966). The outdated and current
understanding of components of the avian telencephalon in
comparison to that of mammals is shown in Fig. 4. Immunos-
taining with an antibody to tyrosine hydroxylase (TH) clearly
demonstrated that the avian basal ganglia did not occupy
the majority of the telencephalon as suggested by Nissl stain-
ing (Figs. 4 and 5C) rather it occupied the ventromedial region
similar to mammals (Figs. 4B, D). The avian dorsal somatomo-
tor basal ganglia and its major structures in relation to the
pallium are shown in Figs. 4D and 5. Details of each of its com-
ponents (medial striatum, lateral striatum, globus pallidus,
and intrapeduncular nucleus) which have been more exten-
sively studied than other parts of the avian subpallium are
reviewed below. In this section, we also discuss area X of the
songbird medial striatum.
3.1.1. Medial striatum
The medial striatum (MSt) together with the lateral striatum
(LSt) has been known for many years to share numerous neu-
rochemical, developmental and hodological traits with the
mammalian dorsal striatum, and on this basis (including the
Fig. 5 –Images of transverse sections of pigeon brain
immunolabeled for A. Substance P (SP) and B. Choline
acetyltransferase (ChAT). Transverse section of chicken brain
immunolabeled for C. Tyrosine hydroxylase (TH). Note the
enrichment of the ventral pallidum (VP) in SP fibers and ChAT
neurons and the paucity of SP fibers and relative paucity of
ChAT neurons in the lateral part of the bed nucleus ofthe stria
teriminalis (BSTL). In B, the field of cholinergic neurons
spanning the VP and lateral forebrain bundle (LFB) represents
the basal magnocellular cholinergic cell group (NBM). Image C
shows the enrichment of striatal parts of the basal ganglia in
fibers containing TH, and identifies the parts of the dorsal
somatic basal ganglia. Abbreviations: GP = globus pallidus;
LSt —lateral striatum; MSt = medial striatum; SL = lateral
septal nucleus; TSM = tractus septopallio-mesencephalicus.
Scale bar= 1 mm in A and C (scale bar in A applies to A, B). See
list of abbreviations for other abbreviations shown in this
figure.
75BRAIN RESEARCH 1424 (2011) 67–101

presence of similar structures in reptiles) considered to be ho-
mologous to the mammalian caudate-putamen (Reiner et al.,
2004a). The MSt and LSt differ in their connectivity, and are
not considered strictly homologous to caudate and putamen,
respectively, in a one-to-one manner. Thus, the MSt and LSt
need to be discussed separately. In addition to embryological
origin, shared traits that show MSt and LSt are striatal which
include a neuropil rich in acetylcholinesterase (AChE), choline
acetyltransferase-containing terminals (ChAT; Medina and
Reiner, 1994), dopamine (DA) —containing terminals (revealed
by TH immunostaining), substance P (SP) —containing peri-
karya and processes, and enkephalin (ENK) —containing peri-
karya and processes (Fig. 5; reviewed in Reiner et al., 1998a).
Concordant with its rich dopaminergic innervation, MSt and
LSt have also been shown to be rich in D1
A
,D1
B
, and D2 dopa-
mine receptors (Casto and Ball, 1994; Dietl and Palacios,
1988; Kubikova et al., 2010; Richfield et al., 1987; Schnabel
and Braun, 1996; Schnabel et al., 1997; Stewart et al., 1996; Sun
and Reiner, 2000), and the dopamine receptor signaling pro-
tein DARPP32 (Bálint et al., 2004; Reiner et al., 1998b). Associ-
ated with its rich cholinergic innervation, MSt and LSt are
rich in muscarinic receptors (Dietl et al., 1988; Kohler et al.,
1995; Wächtler and Ebinger, 1989). In these regards, MSt re-
sembles mammalian striatum, as well as in the expression
of the developmentally regulated genes noted above.
One underlying reason for the neurochemical similarity be-
tween avian MSt and mammalian striatum is that they consist
of the same major neuron types. This includes GABAergic pro-
jection neurons, which make up the bulk of MSt neurons.
These projection neurons possess spiny dendrites, and about
half also contain enkephalin while the other half show co-
localization of substance P (SP) and dynorphin (Anderson and
Reiner, 1990a, 1991; Brauth et al., 1983; Reiner and Anderson,
1990; Reiner et al., 1983, 1984; Sun et al., 2005; Veenman and
Reiner, 1994). These neurons account for the SP+ and enkepha-
linergic projections of MSt to the dopaminergic neurons of the
substantia nigra pars compacta and the GABAergic neurons of
the substantia nigra pars reticulata (Anderson et al., 1991; Medina
et al., 1995; Veenman and Reiner, 1994), of which the SP+ projec-
tion is more prominent. The MSt neurons projecting to the sub-
stantianigraandtheventraltegmentalareasendtheiraxons
through the ventral pallidum, and some have terminations
there (Kitt and Brauth, 1981; Medina and Reiner, 1997; Person
et al., 2008). Interneurons make up most of the remainder of
MSt neurons, although the percent projection neuron versus
interneuron composition of MSt is not certain. The interneurons
include: (1) large, aspiny cholinergic neurons that contain choline
acetyltransferase (Medina and Reiner, 1994); (2) medium-sized
aspiny GABAergic interneurons co-localized with somatostatin
and neuropeptide Y (NPY) (Anderson and Reiner, 1990b); and
(3) medium-sized aspiny neurons containing GABA, the
calcium-binding protein parvalbumin, and the neurotensin-
related hexapeptide LANT6 (Reiner and Anderson, 1993; Reiner
and Carraway, 1987). These neurons appear to have similar elec-
trophysiological properties to their mammalian counterparts
(Farries and Perkel, 2000; Farries et al., 2005b). In mammals, a
fourth type of interneuron contains GABA and the calcium bind-
ing protein calretinin (Bennett and Bolam, 1993; Figueredo-
Cárdenas et al., 1996),andthiscelltypeisrareorabsentinbird
MSt (Laverghetta et al., 2005).
One cell type that is present in MSt but absent in mamma-
lian striatum is a neuron type that appears pallidal in its de-
velopmental derivation, neurochemistry, connectivity and
physiology. As noted in the section above, during develop-
ment a massive migration of cells occurs from the pallidal
subdivision into the medial striatum in chickens. These cells
can be recognized as pallidal since they express Nkx2.1,Lhx6
and/or Lhx7/8, and they are distributed throughout MSt and
continuous with the far more concentrated pallidal neurons of
the globus pallidus, which have a similar gene expression sig-
nature (Abellán and Medina, 2009). Some of these neurons de-
rived from the pallidal proliferative zone are likely to constitute
striatal interneurons, such as those containing parvalbumin/
LANT6 or somatostatin/neuropeptide Y (Carrillo and Doupe,
2004; Cobos et al., 2001a). The neurons expressing Nkx2.1,
Lhx6 and/or Lhx7/8 are, however, more numerous than the par-
valbumin/LANT6 or somatostatin/neuropeptide Y interneuron
populations (Abellán and Medina, 2009; Anderson and Reiner,
1990b; Reiner and Carraway, 1987), and at least some of them
may be those shown to project to intralaminar thalamus in
chickens and zebra finches, and possess pallidal electrophysiol-
ogy (Farries and Perkel, 2002; Farries et al., 2005b; Person et al.,
2008; Reiner et al., 2004a). Given the robustness of this trait in
these two avian species, it seems likely that it is a general
trait of MSt in birds. Consistent with this, the MSt in pigeons
is rich in GABAergic woolly fibers that also contain either SP
or enkephalin, especially along its medial wall (Reiner et al.,
1983, 1984, 1998b). The woolly fiber pattern of SP+ and enke-
phalinergic terminal distribution is characteristic of pallidal
neurons but not striatal interneurons. The putative intra-MSt
pallidal neuron dendrite targets of this woolly fiber input are
not rich in parvalbumin or LANT6 (Reiner and Carraway,
1987), and thus the pallidal neurons receiving this input in
MSt have not been reported previously. The developmental
data together with the neuropeptide immunolabeling data sug-
gest that pallidal neurons may be numerous and widespread in
MSt, but low in the conventional pallidal neuron markers par-
valbumin or LANT6, at least in adults. While it is known that
some of these pallidal MSt neurons project to intralaminar
thalamus, it is unknown if they have other projection targets
as well.
The MSt also evidences a medial-lateral difference in
neurochemical traits and connectivity. For example, medial
MSt receives its dopaminergic input from the A10 dopami-
nergic neurons of the ventral tegmental area (VTA, Figs. 6A,
B) (Bailhache and Balthazart, 1993; Kitt and Brauth, 1986b;
Puelles and Medina, 1994; Reiner et al., 1994), while more lat-
eral MSt receives its dopaminergic input from the A9 dopami-
nergic neurons of the substantia nigra pars compacta (SNc,
Figs. 6A, C; Bailhache and Balthazart, 1993; Durstewitz et al.,
1998, 1999; Karle et al., 1996; Kitt and Brauth, 1986b; Medina
and Reiner, 1995; Metzger et al., 1996; Puelles and Medina,
1994; Reiner et al., 1994, 1998a,b; Smeets and Reiner, 1994;
Székely et al., 1994). Similar parcellation has been observed
in the preferential origin of the projections to the ventral
tegmental area or substantia nigra from the medial versus
lateral MSt, respectively (Mezey and Csillag, 2002). The MSt
also receives major excitatory afferents from pallial regions.
As in mammals, the “corticostriatal”projection utilizes gluta-
mate, an excitatory amino acid neurotransmitter (Csillag et
76 BRAIN RESEARCH 1424 (2011) 67–101

al., 1997; Ding and Perkel, 2004; Ding et al., 2003; Farries et al.,
2005a; Reiner et al., 2001; Veenman and Reiner, 1996). More
lateral MSt receives pallial input from somatic regions, such as
those involved in somatosensory, visual, auditory and motor
function (Brauth et al., 1978; Karten and Dubbeldam, 1973; Notte-
bohm et al., 1976; Veenman et al., 1995; Wild, 1987; Wild et al.,
1993). By contrast, medial MSt appears more viscerolimbic,
since its pallial input arises from such regions as hippocampus
and olfactory bulb. Similarly, its excitatory thalamic input also
arises from midline, more viscerolimbic intralaminar nuclei
than does that to lateral MSt (Veenman et al., 1997). Thus, the
two parts of MSt may differ in function, with medial MSt more
viscerolimbic than lateral MSt. One possibility is that medial
MSt is comparable to mammalian striosomes, since both are
poor in calbindin (Bálint and Csillag, 2007; Roberts et al., 2002).
Abellán and Medina (2009), however, have suggested that birds
may lack the part of the dorsal striatal proliferative zone that
gives rise to striosomes. Thus, the medial MSt viscerolimbic
traits may be comparable to those of medial mammalian cau-
date. Nonetheless, MSt seemingly differs from mammalian cau-
date in that its striatal neurons mainly project to the nigra and
very few to globus pallidus. Additionally, a ventral and caudal
part of what has been termed MSt may be part of the viscerolim-
bic striatum comparable to part of the shell of nucleus
Fig. 6 –Sources of afferent inputs to the basal ganglia in chick brain. A. Brain atlas plate A3.4 (Kuenzel and Masson, 1988).
Boxed areas show locations of images 6B and 6C. B. Ventral tegmental area (VTA) or A10 dopaminergic cell group. Scale
bar= 200 μm. C. Substantia nigra pars compacta (SNc) or A9 dopaminergic cell group. Scale bar =200 μm. D. Chick brain atlas
plate A2.4; boxed area shows location of photomicrograph 6E. E. A8 dopaminergic cell group. Scale bar=200 μm. F. Chick brain
atlas plate A1.4. Boxed area shows location of photomicrograph 6G. G. Locus coeruleus or A6 noradrenergic cell group. Scale
bar= 100 μm. Neurons in figure immunolabeled with antibody to tyrosine hydroxylase.
77BRAIN RESEARCH 1424 (2011) 67–101

accumbens (Abellán and Medina, 2009). This region, however,
may not be strictly equivalent to mammalian accumbens shell
since unlike shell it is very rich in cholinergic neurons, dopami-
nergic terminals and SP+ and ENK+ woolly fibers. Accumbens
core and shell are discussed in more detail in the viscerolimbic
section.
3.1.2. Lateral striatum
As noted above, the LSt of birds possesses the neurochemistry
and many of the neuron types characteristic of mammalian
dorsal striatum, including neuropil enrichment in AChE, cho-
line acetyltransferase-containing terminals, SP+ neurons, enke-
phalinergic neurons, D1, D1
A
,D1
B
, and D2 dopamine receptors,
DARPP32 and muscarinic receptors. As true of MSt, the dopa-
mine receptors and DARPP32 enrichment in LSt reflect the
prominent dopaminergic input, in this case from the substantia
nigra pars compacta (Figs. 6A, C) and A8 (Figs. 6D, E) tegmental
cell groups. The LSt, except for its lateral edge, which may be-
long to the olfactory tubercle, receives its excitatory input main-
ly from somatic pallial and thalamic regions (Veenman et al.,
1995, 1997). This feature of its input is consistent with its output
circuitry to the globuspallidus, which gives rise to an output to
motor pallium in the Wulst (thought to be an M1 homologue)
via the avian motor thalamus (the ventrointermediate area, or
VIA). The LSt neurons giving rise to this are likely to be SP+,
and one of the so-called “direct pathway”outputs of the stria-
tum for facilitating movement (Jiao et al., 2000). The enkephali-
nergic neurons of the LSt, by contrast, have been shown to give
rise to the “indirect pathway”out of the avian striatum, which
projects to pallidal neurons innervating thesubthalamic nucle-
us (Jiao et al., 2000; Person et al., 2008). This circuit appears to be
involved in suppressing unwanted movements, as also the case
in mammals (Jiao et al., 2000). With respect to its motor role as
well as its presumed output to pallidal neurons projecting to
intralaminar thalamus, the LSt may be comparable to the dor-
solateral mammalian striatum. Moreover, the striatal neurons
of primate dorsolateral striatum more heavily project to the
globus pallidus than to nigra (Lévesque and Parent, 2005; Parent
et al., 1995), as is also true of avian LSt. While at one time it
seemed the avian LSt had no projections to the substantia
nigra, recent evidence shows that some LSt neurons project to
substantia nigra pars compacta and pars reticulata (Mezey and
Csillag, 2002; Person et al., 2008).
Although the LSt contains most of the same striatal neuron
types as the MSt, there are some notable differences. For exam-
ple, while the LSt contains abundant SP+ spiny projection neu-
rons, ENK+ spiny projection neurons and parvalbuminergic
interneurons, immunolabeling suggests that LSt contains far
fewer cholinergic and SS/NPY interneurons than MSt (Anderson
and Reiner, 1990b; Medina and Reiner, 1995; see Fig. 6 and 13 in
Abellán and Medina, 2009) or they may even be absent (Person
et al., 2008). Nonetheless, the LSt is rich in cholinergic terminals
and muscarinic receptors (Dietl et al., 1988; Kohler et al., 1995;
Medina andReiner, 1995; Wächtler and Ebinger, 1989). Addition-
ally, in situ hybridization for ChAT mRNA in day-old hatching
chicks reveals some LSt cells positive for ChAT (Abellán and
Medina, 2009), although the labeling is weaker than in MSt. It
may be that immunostaining does not effectively label the
somata of these cells or perhaps there is a developmental
change in ChAT expression. Regardless, it is possible that the
sparse and weaklylabeled somata of LSt give rise to a densecho-
linergic innervation. Alternatively, cholinergic neurons of MSt,
globus pallidus or the intrapeduncular nucleus (see below)
could provide the cholinergic innervation to LSt. Cholinergic in-
nervation is important in regulating striatal projection neuron
function and synaptic plasticity (Kreitzer and Malenka, 2008).
The paucity of unambiguous resident cholinergic neurons in
LSt (i.e. motor striatum) in birds indicates that the role of cholin-
ergic neurons in striatal plasticity may differ from that in mam-
mals. The functional implication of the apparent absence of
somatostatinergic/NPY+ interneurons in LSt is uncertain.
3.1.3. Intrapeduncular nucleus
The intrapeduncular nucleus (INP), located below the inferior
margin of the avian globus pallidus, is named for its location
within the lateral forebrain bundle. Karten and Dubbeldam
(1973) originally thought that its position resembled that of the
mammalian internal pallidal segment, but subsequent immuno-
labeling studies showed that it lacked the pallidal-type neurons
and the SP/DYN-containing striatal input characteristic of the in-
ternal pallidal segment (Anderson and Reiner, 1990a; Reiner and
Carraway, 1987; Reiner et al., 1983, 1999; Veenman and Reiner,
1994). More recent studies have shown that the INP contains
densely packed GABAergic spiny neurons that express
DARPP32 (Reiner et al., 1998b; Schnabel et al., 1997; Sun et al.,
2005), and a very similar glutamate receptor profile to the stria-
tum (Wada et al., 2004). Moreover, the INP has recently been
found to develop from the ventralmost striatal progenitor zone,
to show continuity with the medial striatum, and to contain neu-
rons expressing Lmo4 and cell-surface proteins (Cadherin-8)
characteristic of striatal neurons (Abellán and Medina, 2009).
The striatal neurons of INP include both SP-containing and enke-
phalinergic neurons. It also contains neurons derived from the
pallidal and preoptic proliferative zones (identifiable as expres-
sing Lhx6 and/or Lhx7/8), as typical of the medial and lateral stri-
atum proper (Abellán and Medina, 2009). The INP neurons
expressing Lhx6 and/or Lhx7/8 may include the many cholinergic
neurons and the few parvalbuminergic/LANT6 neurons it
contains (Medina and Reiner, 1994; Reiner and Carraway,
1987). Like LSt, INP is poor in somatostatin/NPY interneurons
(Anderson and Reiner, 1990b). Although the data thus suggest a
largely striatal nature for the INP, it also possesses some traits
that differ from those of MSt and LSt. For example, INP is
much richer than either MSt or LSt in LAMP, a limbic system
marker (Yamamoto and Reiner, 2005), which is consistent
with its derivation from the ventralmost partof the striatalsec-
tor of the developing subpallium, from which much of limbic
striatum derives. The INP also contains many more immigrant
cholinergic neurons than either MSt or LSt (Abellán and Medina,
2009). These cholinergic neurons appear to belong to the corti-
copetal system (Medina and Reiner, 1994). Finally, although
seemingly a striatal territory, the INP is poor in dopaminergic
terminals and dopamine receptors, making its enrichment in
DARPP32 somewhat puzzling.
Given then that INP is a striatal derivative containing neu-
rons with striatal traits, on what basis should it be assigned to
dorsal striatum rather than ventral striatum, especially with
its derivation from the ventral part of the striatal proliferative
zone and its enrichment in LAMP? The relevant feature of INP
that warrants this classification is that the INP is part of the
78 BRAIN RESEARCH 1424 (2011) 67–101

circuitry controlling motor function via descending motor
projections to the midbrain tectum. Karten and Dubbeldam
(1973) had suggested that both globus pallidus and INP might
project to the lateral spiriform nucleus of the pretectum (SpL).
In later studies, SpL was found to project to deep layers of the
optic tectum (Reiner et al., 1982a,b), and its neurons were
shown to have pallidal morphology and neurochemistry (Reiner
and Anderson, 1993; Reiner and Carraway, 1987; Veenman and
Reiner, 1994). At that time, retrograde labeling with horseradish
peroxidase only confirmed the GP projection to SpL but not the
INP projection. More recent studies using biotinylated dextran
amine (BDA) as the tracer have shown that neurons in INP
give rise to a descending projection through the diencephalon
(Jiao et al., 2000). Recent studies indicate that neurons in INP
as well as some in LSt project to the SpL (Reiner and Medina,
unpub. obs). The LSt flanking the INP receives a major projec-
tion from the internal division of the entopallium, a thalamore-
cipient zone, within the telencephalon, of the tectofugal visual
system (Krützfeldt and Wild, 2005). The neurons in LSt at least
contain SP, and are thus direct pathway neurons. SpL also re-
ceives input from globus pallidus neurons (Medina and Reiner,
1997; Reiner et al., 1982a), which themselves receive input
from enkephalinergic LSt neurons (Reiner and Medina, unpub.
obs.). These results indicate that the INP striatal neurons, to-
gether with SP+ neurons of LSt give rise to a “direct pathway”
type output to SpL (Reiner et al., 1998a). A facilitatory role in tec-
tally mediated head and eye movements seems likely for this
circuit, based on its connectivity.
3.1.4. Globus pallidus
The globus pallidus (GP) in both mammals and birds is neuro-
chemically distinct fromstriatum. For example, the globus palli-
dus has a low densityof dopaminergicand cholinergic terminals
and little acetylcholinesterase (Karten and Dubbeldam, 1973;
Reiner et al., 1994). Correspondingly, it is poor in dopaminergic
and muscarinic receptors (Casto and Ball, 1994; Dietl and
Palacios, 1988; Dietl et al., 1988; Kohler et al., 1995; Kubikova
et al., 2010; Richfield et al., 1987; Schnabel and Braun, 1996;
Schnabel et al., 1997; Stewart et al., 1996; Sun and Reiner,
2000; Wächtler and Ebinger, 1989). The globus pallidus in
birds and mammals is distinguished by the presence of
large, aspiny GABAergic neurons, many of which also contain
parvalbumin and LANT6 (Reiner and Anderson, 1993; Reiner
and Carraway, 1987; Veenman and Reiner, 1994), and a dense
mat of woolly fiber terminals containing GABA and SP, or
GABA and enkephalin, whichend on the aspiny GABAergic neu-
rons (Reiner et al., 1998a). The pallidal neurons are rich in recep-
tor types related to their predominant inputs. For example, the
pallidal neurons of GP are rich in GABA receptors, as a conse-
quence of their GABAergic input from LSt (Veenman et al.,
1994). Similarly, as a consequence of the glutamatergic input
from subthalamic nucleus, pallidal GP neurons are rich in
NMDA-type and AMPA-type glutamate receptors (Jiao et al.,
2000; Laverghetta et al., 2005; Wada et al., 2004).
The GABAergic neurons of the globus pallidus co-
containing parvalbumin, which represent the majority of pal-
lidal neurons in mammals and birds, derive from the pallidal
progenitor zone (Abellán and Medina, 2009; Nóbrega-Pereira
et al., 2010; Xu et al., 2008). In mammals, globus pallidus neu-
rons remain in situ relatively near the lateral ventricle and
inferior and medial to the striatum. In birds, the pallidal neu-
rons migrate as a stream from their ventral position, sweep-
ing along an arching ventromedial to dorsolateral course to
invade the striatal sector between INP and LSt to form the glo-
bus pallidus (Abellán and Medina, 2009; Puelles et al., 2007).
Some pallidal neurons remain in residence along this course,
and one medial and ventral cluster forms the ventral palli-
dum. Nonetheless, the neurons of the globus pallidus and
ventral pallidum derive from different sectors of the pallidal
anlage, as noted above (Abellán and Medina, 2009). The entire
migratory course of the pallidal neurons remains poor in
striatal markers in adult birds, and largely contains a mix of
pallidal GABAergic neurons and cholinergic neurons. The
migration of pallidal neurons to the globus pallidus is, howev-
er, not precise and many pallidal neurons come to reside in
MSt as well, as noted above. One consequence of pallidal inva-
sion into a lateral striatal territory is that some striatal neu-
rons remain in residence in the formerly striatal territory
that has been “taken over”by pallidal neurons to create
avian globus pallidus. Hence, SP+ and enkephalinergic spiny
neurons are present in low abundance in avian GP (Abellán
and Medina, 2009; Molnar et al., 1994; Reiner et al., 1983,
1984). In mammals, the globus pallidus also contains a sub-
population of enkephalinergic neurons, which have descend-
ing projections with collaterals to the striatum (Hoover and
Marshall, 1999, 2002; Kita and Kita, 2001). The embryonic origin
of these cells may be the striatal subdivision (Nóbrega-Pereira
et al., 2010). In mice, this pallidal subpopulation is GABAergic,
but does not express the pallidal gene Nkx2.1, and is spared
in Nkx2.1 knockout mouse (Nóbrega-Pereira et al., 2010), in
which the pallidum is missing (Sussel et al., 1999). On the
other hand, the cholinergic neurons that invade the pallidum
are derived from the preoptic subpallial subdivision (POC) in
both mouse and chicken (Abellán and Medina, 2009; García-
López et al., 2008; Nóbrega-Pereira et al., 2010). Since these
neurons belong to the corticopetal system, they will be treated
in a later section.
The globus pallidus in mammals consists of two distinct
segments that differ in the type of striatal neuron from
which they receive input, and that differ in their projection
targets. The external pallidal segment (GPe) receives enkepha-
linergic striatal input (from indirect pathway striatal neurons)
and projects mainly to the subthalamic nucleus (STN), tha-
lamic reticular nucleus and the substantia nigra pars reticu-
lata, while the internal pallidal segment (GPi) receives SP+
striatal input (from direct pathway striatal neurons) and pro-
jects mainly to intralaminar and motor thalamus. In birds,
the globus pallidus is a singular structure that contains both
of these pallidal neuron types, as evidenced by the overlap
of SP+ and enkephalinergic inputs to the avian GP and as evi-
denced by the projection of the avian GP to the targets of both
the mammalian GPe and GPi (Medina and Reiner, 1997). These
projections have been detailed in prior papers (e.g. Farries et
al., 2005a; Medina and Reiner, 1997) and will be discussed in
the following section on functional organization of the avian
basal ganglia.
3.1.5. Functional considerations for dorsal basal ganglia
Models of the functional organization of the somatic basal
ganglia in mammals have recognized two parallel output
79BRAIN RESEARCH 1424 (2011) 67–101

circuits that have opposing functions in motor control and
that interact with one another. These two output circuits orig-
inate from differing sets of striatal neurons and are called the
indirect (from enkephalinergic striatal neurons) and direct
pathways (from SP+ striatal neurons) (Albin et al., 1989;
Delong, 1990; Gerfen, 1992). The connections and functions
of these two circuits have been detailed elsewhere and will
not be reviewed here. Notably, the structure comprising the
dorsal basal ganglia in birds is organized functionally into
similar direct and indirect pathways. This too has been
Fig. 7 –The songbird anterior forebrain circuit. A. A simplified, neuroanatomical schematic representation of the avian song
system. The direct motor pathway arises from nucleus HVC (proper name), which projects to the robust nucleus of the
arcopallium (RA), which in turn projects to the tracheosyringeal half of the hypoglossal nucleus (nXIIts) and other respiratory
premotor neurons in the brainstem. Another projection from HVC leads to area X of the MSt. Area X projects to the medial
portion of the dorsolateral nucleus of the thalamus (DLM), which projects to the lateral magnocellular nucleus of the anterior
nidopallium (LMAN). LMAN sends a projection to RA, with axon collaterals projecting to area X. As part of the MSt, area
X receives a strong dopaminergic input from the ventral tegmental area (VTA). Axon collaterals of the area X projection to DLM
terminate in the ventral pallidum (VP), an area that sends projections to the region of the dopaminergic midbrain (VTA) that
ultimately projects to area X. B. Combined electrophysiological and cellmorphological classification of neurons of area X. There
are four classes of neurons that correspond to mammalian striatal neurons: spiny neurons; cholinergic; fast spiking (FS); and
low-threshold spiking (LTS). In addition, there is a neuron with pallidal properties, an aspiny fast firing cell (AF).
Images and traces from Farries and Perkel (2002).
80 BRAIN RESEARCH 1424 (2011) 67–101

reviewed extensively elsewhere, and the circuit details will
not be repeated here (Reiner et al., 1998a). Of present interest
are two major ways in which the direct–indirect pathway
plan differs between birds and mammals. First, while mam-
mals have two SP+ direct output pathways (to GPi and to the
SNr), birds possess three, one from MSt SP+ neurons to SNr,
one from LSt SP+ neurons to GPi-type neurons of globus palli-
dus, and one from presumptive SP+ neurons of LSt and INP to
SpL. Secondly, it is not yet certain how the pallidal neurons of
MSt fit into this circuit diagram. It is known that some of these
neurons project to intralaminar thalamus, but it is unknown if
they have additional projection targets, such as STN or SNr.
Since both SP+ and enkephalinergic woolly fibers are present
in MSt, it seems likely that MSt pallidal neurons include both
GPe-type and GPi-type pallidal neurons. Despite these differ-
ences, the similarities between mammals and birds in the func-
tional organization of the dorsal basal ganglia are extensive.
Lesion studies and pharmacological manipulations in birds re-
inforce this view (Cheng and Long, 1974; Goodman and Stitzel,
1977; Goodman et al., 1982, 1983; Koster, 1957; Rieke, 1980,
1981, 1982; Sanberg and Mark, 1983; Schwarcz et al., 1979).
Given these data and that avian species are similar to humans
in being bipedal, warm-blooded, and capable of complex
motor behaviors that can be readily measured, birds can poten-
tially serve as useful models to explore the pathophysiology of
basal ganglia-related disorders such as Parkinson's disease,
Huntington's disease,obsessive–compulsive disorder and Tour-
ette syndrome.
3.1.6. Area X: A specialized songbird striatal structure
The role of the anterior forebrain pathway (AFP) in song learn-
ing in songbirds has become of significant interest to basal
ganglia researchers, due to the involvement of a specialized
part of the songbird basal ganglia in this circuit. The serially
connected components of the AFP include the following: nu-
cleus HVC (proper name) of the pallium; area X of the MSt;
the medial portion of the dorsolateral thalamic nucleus
(DLM), a specialized intralaminar thalamic nucleus; and the
lateral magnocellular nucleus of the anterior nidopallium
(LMAN). These nuclei are serially connected with strictly ipsi-
lateral projections (Fig. 7A). Moreover, area X, like the sur-
rounding striatum, receives a strong dopaminergic input
from the substantia nigra and VTA (Figs. 6A–C; Bottjer, 1993;
Gale and Perkel, 2005; Soha et al., 1996). The AFP is required
for song learning and adult song plasticity. Therefore its role
appears comparable to that of cortico–basal ganglia–cortical
circuits in the learning and execution of motor sequences in
mammals (Bottjer et al., 1989; Brainard and Doupe, 2000;
Scharff and Nottebohm, 1991; Sohrabji et al., 1990; Williams
and Mehta, 1999; reviewed in Doupe et al., 2005). Reinforcing
this notion is the observation that the language-related gene
of humans FoxP2 is expressed at very high levels in striatum
and area X (Fisher and Scharff, 2009; Haesler et al., 2004,
2007; Teramitsu et al., 2004; White et al., 2006).
Area X contains a full complement of neurons typical of stri-
atum such as spiny neurons, cholinergic interneurons, parval-
buminergic interneurons and somatostatinergic interneurons
(Farries and Perkel, 2002; Reiner et al., 2004a). As true of stria-
tum, the vast majority of area X neurons are spiny neurons
and essentially identical electrophysiologically to mammalian
striatal spiny projection neurons (Fig. 7B; Farries and Perkel,
2002). In the zebra finch brain, high expression of D1A, D1B
and D2 dopamine receptors has been found in striatum, includ-
ing area X. Within area X, 77% of neurons expressed D1A, 70%
expressed D2, and half appear to express both D1A and D2 re-
ceptors (Kubikova et al., 2010). As noted above, area X receives
a“corticostriatal”input from the HVC (Ding and Perkel, 2004;
Ding et al., 2003; Farries et al., 2005b). In contrast to any part of
striatum that has been described in any mammalian species,
however, area X projects directly to the thalamus (Bottjer
et al., 1989; Okuhata and Saito, 1987; Parent and Hazrati, 1995).
In mammals, it is a pallidal structure of the basal ganglia, the
globus pallidus that projects to the thalamus. Area X has been
discovered, however, to adhere to this pallidal output rule in a
surprising way. The neurons of area X that project to the medial
dorsolateral nucleus of the anterior thalamus (DLM) are pallidal
in their traits —large, few in number, aspiny and pallidal in
their neurochemistry, electrophysiology (Fig. 7B) and input
from area X spiny neurons (Bottjer et al., 1989; Farries and
Perkel, 2002; Goldberg and Fee, 2010; Goldberg et al., 2010;
Luo and Perkel 1999; Reiner et al., 2004a). The mixing of striatal
and pallidal neurons in area X is not unique to area X in song-
birds, sincethe MSt region surrounding area X also containspal-
lidal neurons projecting to the DLM (Farries et al., 2005b; Reiner
et al., 2004a).It is important to note, however, that not all prop-
erties of area X pallidal neurons are typical of those in mamma-
lian pallidum. For example, area X neurons that project to DLM
express enkephalin (Carrillo and Doupe, 2004). As noted above,
chicken MSt also contains pallidal neurons, as part of the after-
math of the extensive migration of pallidal neurons dorsally to-
ward GP during development. In this light then, the mixing of
spiny striatal and pallidal aspiny neurons is not unique to area
X of songbirds, but is instead a seemingly widespread feature
of avian MSt. Songbird area X also projects to the ventral palli-
dum, via collaterals of axons projecting to the thalamic nucleus
DLM, which then provides a route by which area X can modu-
late dopaminergic input back to itself during song learning
and modification —ventral pallidum projects to regions of the
ventral tegmental area and substantia nigra pars compacta
that project back to area X (Gale and Perkel, 2010; Gale et al.,
2008).
The key qualitative difference between area X and medial
striatum is the apparent lack of an extrastriatal projection of
the spiny neurons of area X. In MSt in zebra finches, chickens
and pigeons, spiny neurons project to extrastriatal targets, as
in mammalian striatum. To date, no substantial projection
beyond area X itself has been identified for area X spiny neu-
rons (Person et al., 2008). Instead, they contact and inhibit pal-
lidal projection neurons within area X (Farries et al., 2005a,
2005b; Reiner et al., 2004a). The fraction of pallidal area X neu-
rons that project to DLM versus VP remains uncertain (Farries
et al., 2005a, 2005b; Goldberg and Fee, 2010; Leblois et al., 2009;
Reiner et al., 2004a).
Finally, we have tentatively grouped area X with somatic
striatum because of its location in rostrolateral MSt, a somatic
territory, and its role in a somatic motor function, song learn-
ing and in modulating song variability during learning
(Ölveczky et al., 2005) or in adulthood (Kao et al., 2005; Leblois
et al., 2010). The interconnections of area X with ventral palli-
dum and VTA raise the possibility that it is perhaps allied with
81BRAIN RESEARCH 1424 (2011) 67–101

viscerolimbic striatum. More detail on its developmental der-
ivation from the striatal proliferative zone and on its neuro-
chemistry (e.g. LAMP) is needed to judge its classification as
somatic, viscerolimbic, or mixed.
3.2. Ventral viscerolimbic basal ganglia
The ventral (viscerolimbic) basal ganglia in mammals pos-
sesses similar subdivisions, neurochemistry and input–
output relations to that of the dorsal somatomotor basal
ganglia. For example, it too consists of striatal subdivisions
(nucleus accumbens and superficial olfactory tubercle) rich
in spiny GABAergic projection neurons containing either sub-
stance P or enkephalin, and a pallidal subdivision (ventral
pallidum and deep olfactory tubercle) to which the striatal
subdivision projects. As true of the dorsal basal ganglia, the
striatal part of the ventral basal ganglia receives pallial and
dopaminergic input, and the pallidal part gives rise to major
outputs of the ventral basal ganglia. Unlike dorsal basal gang-
lia, the inputs and outputs of the ventral basal ganglia are
more related to visceral brain regions and functions. Consis-
tent with this, the ventral basal ganglia appears more in-
volved in reward and motivation underlying appetitive
behavior (Groenewegen and Uylings, 2000; Kelley, 1999). De-
spite the many similarities to dorsal basal ganglia cellular or-
ganization and connectivity, and a basic understanding of
the role of the ventral basal ganglia in reward-based behavior
and functions, neuronal circuit models akin to those for the
somatic basal ganglia have not yet been developed to provide
a neuronal circuit-level explanation for the functions of the
ventral basal ganglia. As reward-motivated processes are a
fundamental attribute of vertebrate behavior, it is not sur-
prising that birds too possess a viscerolimbic basal ganglia
(Reiner et al., 2004b). Although no distinct cytoarchitectonic
boundary distinguishes the dorsal and ventral basal ganglia,
the ventral basal ganglia in both mammals and birds, none-
theless, can be distinguished from the dorsal basal ganglia
by a number of neurochemical distinctions, as detailed
below. The components of the avian viscerolimbic basal
ganglia including the olfactory tubercle, nucleus accumbens
and ventral pallidum were recognized by the Avian Brain No-
menclature Forum, but several gaps in the understanding of
thesestructureswerenotedandsomehavesincebeenfilled.
Notably, the boundaries for structural components are more
clearly e stablished by developmental and neurochemical stud-
ies, including a distinction between the two main subdivisions
of nucleus accumbens. Additionally, it is now evident that, like
in mammals, the avian olfactory tubercle possesses striatal
and pallidal subdivisions.
3.2.1. Olfactory tubercle
The olfactory tubercle (TuO) in mammals forms a prominent
bulge (hence the term tubercle) at the base of the telencepha-
lon, and is distinguished from other structures of the viscero-
limbic basal ganglia by its prominent olfactory bulb input. The
most ventral part of the olfactory tubercle that receives olfac-
tory bulb input in mammals is striatal in derivation, neuro-
chemistry and cytology, while a deeper lying portion is
pallidal. This deeper lying pallidal part of the olfactory tuber-
cle is cytoarchitectonically continuous with the ventral palli-
dum (see below). The striatal part of TuO contains medium-
sized spiny neurons, as typical of striatal subpallium, and
the medium-sized neurons project to the deeper lying pallidal
TuO neurons and to the ventral pallidum (Alheid and Heimer,
1988; Heimer et al., 1976). The small-celled islets of Calleja in-
terposed between the pallidal and striatal parts of the olfacto-
ry tubercle (Puelles et al., 2007) are derived from Lmo4-
expressing neurons of the dorsalmost part of the LGE (Abellán
and Medina, 2009). A ventral subpallial region receiving olfac-
tory bulb input also is present in birds (Reiner and Karten,
1985), although it does not form a distinct ventral telencephal-
ic bulge (Figs. 8A, B). The Nomenclature Forum recognized this
as the olfactory tubercle in birds, noted its hodological and
neurochemical similarities to mammalian olfactory tubercle,
and described it as striatal in nature (Reiner et al., 2004b).
Recent developmental studies suggest, however, that the
TuO in birds has both striatal and pallidal domains (Abellán
and Medina, 2009; Puelles et al., 2000, 2007). Based on the
expression of Pax6 and Lmo4, but the absence of Nkx2.1,Lhx6,
Lhx7/8, and Shh, the rostral and dorsolateral parts of the olfac-
tory tubercle appear to be striatal derivatives, arising from
the avian homologues of mammalian LGE1 and LGE3/LGE4,
respectively. The transcription factor cLmo4 further identifies
cell aggregates in the striatal part of the avian TuO that
resemble the islands of Calleja, which derive from the homo-
logue of mammalian LGE1 (Abellán and Medina, 2009; Puelles
et al., 2007). By contrast, the caudal and ventrolateral TuO in
birds express pallidal markers reflecting an origin from the
pallidal domain. The striatal nature of rostral and dorsolateral
TuO is consistent with its neurochemistry, since it possesses
numerous medium-sized neurons containing the striatal
spiny projection neuron neuropeptide markers enkephalin
and substance P (Abellán and Medina, 2009; den Boer-Visser
and Dubbeldam, 2002; Molnar et al., 1994; Reiner et al., 1983,
Fig. 8 –Sections of chick brain showing selected structures of
the viscerolimbic basal ganglia (BG). A. Sagittal section near
midline and B. Transverse section showing the ventral
portion of medial striatum (MSt) and tuberculum olfactorium
(TuO). 8B, C, D. Transverse sections of BG depicting major
components of the ventral viscerolimbic BG including the
tuberculum olfactorium (TuO), medial striatum (MSt), and
ventral pallidum (VP). Immunolabeled with antibody to
substance P. Scale bars for 8A–8D =1.0 mm. Refer to list of
abbreviations for names of other structures identified.
82 BRAIN RESEARCH 1424 (2011) 67–101

1984). The striatal TuO has also been shown to contain pre-
sumptive interneurons possessing NADPH-diaphorase and
nitric oxide synthase (NOS), as true in mammals as well
(Brüning, 1993; Brüning et al., 1994; Panzica et al., 1994;
Vincent et al., 1983). The striatal TuO additionally is rich in
calcitonin gene-related peptide (CGRP)-containing fibers in bud-
gerigar and quail (Lanuza et al., 2000; Roberts et al., 2002). Mam-
malian TuO also possesses CGRP+ fibers at rostral levels (Kawai
et al., 1985). Additionally, the striatal TuO has been reported to
be rich in thyroid hormone releasing hormone-containing
fibers in ducks (Jozsa et al., 1988). The pallidal nature of caudal
and ventrolateral TuO in birds is consistent with the many
GABAergic, substance-P containing, and enkephalinergic
fibers and terminals it contains (Veenman and Reiner, 1994),
and the presence of many neurons containing the pallidal
neurotensin-related hexapeptide LANT6 (Reiner and Carraway,
1987). A striato-pallidal connectivity of avian TuO is suggested
by the GABAergic, substance-P containing, and enkephalinergic
fibers and terminals in pallidal TuO. In addition, striato-pallidal
connectivity of avian TuO has been indicated in pigeon by a
projection of striatal TuO to the ventral pallidum (Medina and
Reiner, 1997). The TuO in birds has been shown to have wide-
spread extratelencephalic projections to hypothalamus and
midbrain dopaminergic neurons (Medina and Reiner, 1997), as
also true in mammals. The relative contribution of striatal
and pallidal TuO neurons to downstream projection areas is
uncertain.
Consistent with its striatal nature, the rostral and dorsolateral
TuO receive a dopaminergic input from the ventral tegmental
area and substantia nigra of the midbrain (Figs. 6A–C; Kitt and
Brauth, 1986b; Moons et al., 1994; Panzica et al., 1994, 1996), and
contain numerous receptors and second messengers associated
with this input, including D1A, D1B and D2 dopamine receptors,
and DARPP-32 (Ball et al., 1995; Dietl and Palacios, 1988; Durste-
witz et al., 1999; Sun and Reiner, 2000). In mammals, the piriform
cortex and hippocampal formation are sources of pallial input to
the TuO (Heimer and Wilson, 1975). Similarly, in pigeons the piri-
form cortex has been shown to project to the TuO (Bingman et al.,
1994). The dorsomedial avian hippocampus has been shown to
project indirectly to the avian TuO, projecting to the medial and
lateral septum, with medial (striatal) septum having reciprocal
connections with the TuO (Atoji and Wild, 2004). Other demon-
strated sources of input to striatal TuO in birds include the lateral
bed nucleus of the stria terminalis, the lateral hypothalamic area,
the parabrachial region, the nucleus of the solitary tract, and the
dorsal motor nucleus of the vagus (Arends et al., 1988; Atoji et al.,
2006; Berk and Hawkin, 1985; Wild et al., 1990), structures associ-
ated with the autonomic nervous system. These various inputs
to striatal TuO resemble those reported in mammals. Finally,
avian TuO also contains numerous immigrant pallial/cortical de-
rived glutamatergic neurons, as also true in mammals (Abellán
and Medina, 2009; Abellán et al., 2009; Puelles et al., 2000; Stried-
ter et al., 1998). Their functional significance is unknown.
3.2.2. Nucleus accumbens core and shell
The ventral striatum of mammals contains a prominent stria-
tal structure called the nucleus accumbens. This structure is a
major target of the mesolimbic dopaminergic system and an
important part of the brain reward and motivation circuit.
The nucleus accumbens of rats comprises a central core
(AcC) surrounded on its medial, ventral and lateral sides by a
shell (AcS; Herkenham et al., 1984; Záborszky et al., 1985).
The core and shell were initially identified and distinguished
by the relative enrichment of the core in acetylcholinesterase
and the enrichment of the shell in argyrophilic fibers, respec-
tively (Záborszky et al., 1985). Subsequently, immunolabeling
showed differential labeling for substance P (Zahm, 1989)
and calbindin 28kD (Heimer et al., 1997; Martin et al., 1991;
Voorn et al., 1989; Zahm and Heimer, 1993) in rodents, with
the core poor in substance P-containing fibers and rich in
calbindinergic neuropil, and the shell moderate in substance
P-containing fibers and calbindinergic neuropil. Other
markers for the two sub-territories include calretininergic
and neurotensinergic perikarya, which are relatively enriched
in accumbens shell, and enkephalin and the GABA
A
receptor,
which are enriched in neurons of accumbens core (Zahm,
1999). The accumbens in mammals has also been shown to
have a third sub-territory, a rostral pole (Zahm, 2000; Zahm
and Brog, 1992; Zahm and Heimer, 1993).
Fig. 9 –Transverse sections of chick brain showing nucleus
accumbens (Ac) core (AcC) and shell (AcS) subdivisions
processed with antibodies made to the following
neuropeptides/proteins: A. Substance P (SP), B. Neuropeptide
Y (NPY), C. Dopamine and cAMP-regulated phosphoprotein
(DARPP-32), and D. Calbindin (CB). Scale bars= 500 μm. The
lateral border of AcC is particularly well delineated in section
A, however, the border with the dorsomedial MSt is not
marked clearly. The NPY immunoreactivity (B) is useful for
demarcation of the shell. The putative core is dorsolateral to
the BSTl while the putative shell occurs ventrolateral to the
AcC and BSTl. Refer to list of abbreviations for names of other
structures identified.
83BRAIN RESEARCH 1424 (2011) 67–101

The Nomenclature Forum suggested that the homologue of
mammalian nucleus accumbens resides in the ventromedial
striatum of birds (i.e. ventromedial MSt). Markers to confirm
this and better define the relative locations of the avian accum-
bens core and shell, however, were not available at that time.
More recently, developmental (Abellán and Medina, 2009)and
histochemical/hodological studies (Bálint and Csillag, 2007;
Bálint et al., 2011; Husband and Shimizu, 2011; Roberts et al.,
2002) have helped confirm the location of the avian nucleus
accumbens, and clarify the components that appear homolo-
gous to the mammalian accumbens shell and core (Fig. 9). Spe-
cifically, the accumbens in chickens can be identified as a
rostral ventromedial striatal territory that is derived from the
ventrobasal striatal progenitor zone (LGE4 in mammals), and
then its core subdivision can specifically be recognized as a re-
gion within accumbens at the base of the lateral ventricle that
is very rich in neurons expressing genes for SP,ENK,andNPY,
but moderate in cLmo4 (Abellán and Medina, 2009). By contrast,
the accumbens shell can be identified ventral and lateral to the
core by its enrichment in cLmo4. This shell region has a caudal
extension located medial to the intrapeduncular nucleus, with-
in what has been regarded as ventral MSt. Thus, this caudal ex-
tension appears to be part of accumbens shell in birds (Fig. 3).
There is good agreement among recent neurochemical and
hodological studies regarding the overall boundaries of the
entire nucleus accumbens in birds (Abellán and Medina,
2009; Bálint and Csillag, 2007; Bálint et al., 2011; Husband
and Shimizu, 2011; Roberts et al., 2002) and that a third
accumbens sub-territory, a rostral pole, occurs in birds (Bálint
and Csillag, 2007; Bálint et al., 2011; Husband and Shimizu,
2011) that may be comparable to that in mammals (Zahm
and Heimer, 1993). Projections into the avian nucleus accum-
bens resemble those in mammals, and to some extent define
its proposed subdivisions. For example, the nucleus tractus
solitarius projects prominently to accumbens shell but not
core in mammals. Bálint and Csillag (2007) showed by antero-
grade labeling in conjunction with immunolabeling that the
nucleus tractus solitarius (NTS) also projects to accumbens
in birds, and based on the differential projection within nucle-
us accumbens were able to distinguish an accumbens core-
like region (poor in NTS input) and an accumbens shell-like
region (rich in NTS input). Nucleus accumbens also receives
dopaminergic input from the ventral tegmental area (Kitt
and Brauth, 1981; Mezey and Csillag, 2002), and at least one
study in budgerigars (Roberts et al., 2002) has suggested
that the accumbens shell is especially high in tyrosine
hydroxylase-containing (i.e. dopaminergic) fibers. Finally, a
dense noradrenergic input from the A6 neurons of locus coer-
uleus to nucleus accumbens has been reported (Figs. 6F, G),
ending more heavily in accumbens shell (Bailhache and
Balthazart, 1993; Kitt and Brauth, 1986a; Mello et al., 1998;
Moons et al., 1995; Reiner et al., 1994; von Bartheld and
Bothwell, 1992). By contrast, somatic striatum receives only
modest noradrenergic innervation (Bailhache and Balthazart,
1993; Moons et al., 1995; Reiner et al., 1994).
Bálint et al. (2011) recently showed projections from the
chick AcS are similar to those reported in mammals, including
extensive projections to the lateral preoptic area, substantia
nigra pars compacta, ventral tegmental area, A8 dopaminer-
gic cell group, and moderate projections to the periaqueductal
gray, parabrachial complex and nucleus raphe (Groenewegen
and Russchen, 1984; Usuda et al., 1998; Zahm and Heimer,
1993). Although projections from the avian AcC have been
shown to be more extensive than reported for mammals, par-
ticularly in the caudal brainstem, significant projection areas
comparable to those in mammals have been noted, including
the substantia nigra pars compacta, the A8 dopaminergic cell
group, periaqueductal gray and the ventral tegmental area
(Groenewegen and Russchen, 1984; Usuda et al., 1998; Zahm
and Heimer, 1993).
As pointed out in a recent publication, however, identifica-
tion of subdivisions of avian nucleus accumbens as homologous
to particular accumbens subdivisions in mammals is not unam-
biguous and suggests caution needs to be applied (Husband and
Shimizu, 2011). They note that studies in budgerigars (Roberts
et al., 2002), chickens (Bálint and Csillag, 2007) and pigeons
(Husband and Shimizu, 2011) show that the two regions that
some have identified as avian accumbens core and shell do not
match accumbens core and shell in rats (Bubser et al., 2000;
Tan et al., 1999)orprimates(Brauer et al., 2000)particularly
in the localization of the calcium-binding protein calbindin.
Husband and Shimizu (2011) have, thus, used the designations
ventral (vAc) and dorsal (dAc) to subdivide the avian accumbens,
with their vAc and dAc being topographically comparable to the
accumbens shell (AcS) and accumbens core (AcC), respectively,
of others (Fig. 9). On the other hand, the above noted molecular
developmental, neurochemical, and hodological data and recent
immunohistochemical and tract-tracing studies, support the no-
tion that avian AcS and AcC resemble their similarly named
mammalian counterparts in many regards. While further stud-
ies are needed to evaluate the proposed boundaries and homol-
ogies of the avian accumbens subdivisions with respective
mammalian subdivisions, it may be that the counterparts will
not resemble one another by all neurochemical and hodological
criteria.
The nucleus accumbens in its entirety also receives input
from central components of the autonomic nervous system
such as the lateral hypothalamus (Berk and Hawkin, 1985),
lateral part of the bed nucleus of the stria terminalis (Atoji et
al. 2006), parabrachial nucleus (Wild et al., 1990), nucleus trac-
tus solitarius (Arends et al., 1988; Bálint and Csillag, 2007) and
dorsal motor nucleus of the vagus (Arends et al., 1988).
The avian accumbens also receives input from diverse tel-
encephalic and midbrain regions regarded as limbic struc-
tures, including the hippocampus (Atoji and Wild, 2004; Atoji
et al., 2002; Székely and Krebs, 1996; Veenman et al., 1995),
piriform cortex (Veenman et al., 1995), posterior pallial amyg-
dala (Atoji et al., 2006), and ventral tegmental area (Kitt and
Brauth, 1981; Mezey and Csillag, 2002; Moons et al., 1994).
Pallial input to avian accumbens is likely to be glutamatergic
(Csillag et al., 1997; Ding and Perkel, 2004; Ding et al., 2003;
Farries et al., 2005a; Reiner et al., 2001; Veenman and Reiner,
1996). Consistent with its input from limbic regions of brain,
the nucleus accumbens core and shell in birds are enriched
in the limbic system protein LAMP (Yamamoto and Reiner,
2005).
A‘limbic loop’involving medial regions of pallium (i.e.
mesopallium and nidopallium), subpallium and thalamus has
been described in birds (Husband and Shimizu, 2011). The cir-
cuit consists of a projection from a column of neurons in the
84 BRAIN RESEARCH 1424 (2011) 67–101

medial pallium to the nucleus accumbens, from accumbens to
ventral pallidum (VP), from VP to the anterior dorsomedial tha-
lamic nucleus (DMA), and finally a return projection from DMA
to the medial pallium (Fig. 13 in Husband and Shimizu, 2011).
The restricted part of the medial pallium involved in this ‘limbic
loop’has been proposed to be equivalent to the mammalian
prefrontal cortex (Husband and Shimizu, 2011). This medial
pallial sector apparently corresponds to the medial pallial re-
gion previously shown to be involved in imprinting in chicks
(Bolhuis, 1999; Gruss and Braun, 1996; Horn, 1998; Maier and
Scheich, 1987; Metzger et al., 1998; Thode et al., 2005). Thus,
the pallial part of this loop, as well as the loop itself, is associat-
ed with learning and memory. Nonetheless there are behavior-
al, anatomical and electrophysiological data showing that
another brain region, the caudolateral nidopallium, may be
the equivalent of the avian prefrontal cortex (Güntürkün, 2005;
Waldmann and Güntürkün, 1993).
3.2.3. Ventral pallidum
The ventral pallidum (VP) of mammals is regarded as a medio-
ventral extension of globus pallidus and the viscerolimbic com-
ponent of the striatopallidal system. It occupies a relatively
extensive area in the basal forebrain of rats and primates,
extending ventrally and rostrally from the globus pallidus into
the olfactory tubercle (Alheid and Heimer, 1988). The VP pos-
sesses a number of pallidal traits by which it can be identified,
including enrichment in iron (Switzer et al., 1982), large aspiny
glutamate decarboxylase (GAD)-containing neurons, a dense
mat of terminals containing GAD, and dense mats of terminals
containing enkephalin and SP (Beach and McGeer, 1984; Haber
and Nauta, 1983; Haber and Watson, 1985; Switzer et al., 1982).
The terminals containing GAD, enkephalin and SP possess the
distinctive pallidal woolly fiber morphology of striatopallidal
terminals. The VP field in mammals contains two major neuro-
chemically distinct output neuron types, GABAergic neurons
with descending projections and cholinergic neurons with as-
cending projections within the telencephalon (Bengtson and
Osborne, 1999). The GABAergic VP neurons have their origin in
the pallidal progenitor zone of the developing subpallium, as
do globus pallidus neurons (Xu et al., 2008), while cholinergic
neurons have a preoptic origin (García-López et al., 2008;
Nóbrega-Pereira et al., 2010). The globus pallidus and ventral
pallidum in mammals, however, originate from different parts
of the MGE, with the globus pallidus derived from MGE2/MGE3
and the ventral pallidum arising from MGE4 (precommissural
part of VP) and MGE3 (commissural part of VP). This is similar
in birds, although the commissural part of VP (derived from
MGE3) appears to be missing (Abellán and Medina, 2009).
The VP of birds (Figs. 8C, D) was originally termed the ventral
paleostriatum, and the term was used for a large region that
contained both striatal and pallidal neuron types (Kitt and
Brauth, 1986a). The ventral paleostriatum was identified by
the abbreviation PVT (paleostriatum ventrale) in a chick brain
atlas (Kuenzel and Masson, 1988). Others used the term ventral
pallidum instead, and the Nomenclature Forum officially
renamed PVT as the ventral pallidum (VP). In doing so, the re-
gion definedas the ventral pallidum was narrowed to a territory
exclusively having pallidal neurochemistry (Reiner et al.,
2004b). Developmental studies in chicks have been instrumen-
tal in providing support for the identification of this region as
the ventral pallidum, and the homologue of part of the mam-
malian structure of the same name. Specifically, the VP displays
strong expression for Nkx2.1 (Puelles et al., 2000), Lhx6 and
Lhx7/8 (Abellán and Medina, 2009), which within subpallium
are uniquely expressed by pallidal neurons. Like the avian glo-
bus pallidus, the avian VP is rich in fibers and terminals con-
taining substance P, dynorphin, enkephalin and/or GABA
that represent the terminals of striatal neurons (Anderson and
Reiner, 1990a; Reiner et al., 1983, 1984; Veenman and Reiner,
1994; Veenman et al., 1995). Neurons in the avian VP also pos-
sess a similar glutamate receptor expression profile to that of
neurons in the avian globus pallidus (Wada et al., 2001), as
well as GABA receptors (Veenman et al., 1994). The GABAergic
projection neurons of VP in birds co-contain parvalbumin and
the neuropeptide LANT6 (Reiner and Anderson, 1993; Reiner
and Carraway, 1987; Veenman and Reiner, 1994). As in mam-
mals, the large GABAergic neurons of globus pallidus and ven-
tral pallidum arise from separate parts of the pallidal domain,
with the globus pallidus arising from the region homologous
to mammalian MGE2/MGE3, and the ventral pallidum arising
from the homologue of mammalian MGE4 (Abellán and Medina,
2009). The VP in birds only corresponds to the precommissural
VP of mammals (Abellán and Medina, 2009) and contains a
prominent group of cholinergic neurons, as it does in mammals
(Medina and Reiner, 1994). The cholinergic neurons of avian VP
(and those in globus pallidus and INP) derive from the POC sub-
pallial subdivision (Abellán and Medina, 2009), as also true of
the cholinergic neurons of mammalian VP (García-López et al.,
2008). They constitute a separate system that will be discussed
further in Section 3.4 (Basal telencephalic cholinergic and non-
cholinergic corticopetal system).
As true of globus pallidus, the avian ventral pallidum re-
ceives striatal input (in this case viscerolimbic) and it gives rise
to major descending output to targets very similar to those of
mammalian VP (Medina and Reiner, 1997). Viscerolimbic striatal
structures projecting to VP include the olfactory tubercle and
nucleus accumbens (Medina and Reiner, 1997). The VP in birds
also has been reported to receive pallial inputs from the
temporo-parieto-occipital area and diencephalic inputs from
the lateral hypothalamic area (Atoji and Wild, 2005; Berk and
Hawkin, 1985; Medina and Reiner, 1997; Veenman et al., 1995).
The avian VP, in turn, projects to a number of diencephalic
sites including, the subthalamic nucleus, paraventricular nucle-
us, dorsomedial thalamus, habenular nuclei, thalamic reticular
nucleus, and lateral hypothalamic area (Berk and Hawkin,
1985; Kitt and Brauth, 1981; Medina and Reiner, 1997; Veenman
et al., 1995). Several midbrain regions receive ventral pallidal
input as well, including the ventral tegmental area, substantia
nigra pars compacta, pedunculopontine tegmental nucleus,
central gray, and raphe (Kitt and Brauth, 1981; Medina and
Reiner, 1997).
3.2.4. Functional considerations for ventral basal ganglia
The dopaminergic input to viscerolimbic striatum in mammals,
especially nucleus accumbens, is widelythought to mediate the
rewarding effects of natural stimuli such as food, water and sex
(Salamone et al., 1997). The many autonomic circuit inputs and
outputs of the viscerolimbic basal ganglia are consistent
with such a function. Nucleus accumbens, in particular, plays
a major role in the initiation of reward-motivated behavior
85BRAIN RESEARCH 1424 (2011) 67–101

(Roberts et al., 1980). Because reward provides the motivation
for learning, the nucleus accumbens has also been regarded as
critical for reward- and incentive-based learning (Salamone
et al., 1997). Moreover, drugs of abuse, such as cocaine, amphet-
amine, morphine and methamphetamine, produce their plea-
surable sensations by release of dopamine and increased
neuronal activation in nucleus accumbens, especially the
accumbens shell (Pierce and Kalivas, 1995; Pontieri, et al., 1994,
1995). The dopaminergic input from the posteromedial ventral
tegmental area to the medial olfactory tubercle and ventrome-
dial accumbens shell appears particularly involved in reward,
based on behavioral findings addressing the effects of intra-
accumbens cocaine or amphetamine administration (Ikemoto,
2007). The role of the ventral basal ganglia, however, is
more complex than a simple role in facilitating pursuit of re-
ward (Salamone et al., 1997). Nucleus accumbens also plays a
role in withholding responses so as to maximize reward, and le-
sions of accumbens core impair this ability and cause impulsive
behavior (Cardinal et al., 2001). The nucleus accumbens, espe-
cially the shell, is also responsive to stress (Kalivas and Duffy,
1995; King et al., 1997). Although neural circuit models (e.g. the
direct–indirect pathway model) have been developed to explain
how the somatic basal ganglia mediates motor control at the
neuronal level, how the striatopallidal circuitry of the viscero-
limbic basal ganglia mediates its role in reward-motivated be-
havior, choice and learning is yet to be elucidated at the
neuronal circuit level.
The viscerolimbic basal ganglia in birds appears to be in-
volved in reward, and reward-motivated learning. For example,
Delius et al. (1976) have shown that electrical stimulation of the
accumbens region has rewarding properties in birds, and medi-
al striatal neurons in chick show reward-related responses
(Yanagihara et al., 2001). Similarly, chicks with electrolytic le-
sions of the ventromedial striatum, including the accumbens
region, are impaired in their ability to associate color cues
with reward (Aoki et al., 2006; Izawa et al., 2003). Such lesions
also cause impulsivity in chicks. Additionally, the accumbens
region is associated with passive avoidance learning in chicks
(Stewart et al., 1996). One difficulty in relating the results of
these studies to specific parts of viscerolimbic basal ganglia is
that the stimulating, recording or lesion sites inthe above stud-
ies spanned the somatic and viscerolimbic medial striatum.
Thus, the relative contribution of limbic striatum and medial
MSt to these functions is not certain. As true of medial caudate
in mammals, medial MSt appears to be viscerolimbic in connec-
tivity, function and neurochemistry (Yamamoto and Reiner,
2005). As discussed in the previous section on the nucleus
accumbens, a ‘limbic loop’circuit comprising prefrontal
cortex-like medial pallial neurons, medial MSt/nucleus accum-
bens, ventral pallidum anda mediodorsal-like thalamic nucleus
that may be involved in learning and memory has been demon-
strated in pigeons (Husband and Shimizu, 2011).
3.3. Subpallial amygdaloid nuclei: The extended
amygdala —central and medial amygdala, and bed nuclei of
the stria terminalis
The amygdala in mammals has been recognized as consisting
of two major subpallial cell groups, the central and medial
amygdaloid nuclei (Swanson and Petrovich, 1998). Heimer
and coworkers recognized, however, that these two amygda-
loid nuclei were each confluent with neuronal corridors that
extended from them, through the territory below the globus
pallidus (i.e. sublenticular) to the bed nuclei of the stria termi-
nalis or BST (Alheid and Heimer, 1988; Alheid et al., 1995). The
distinctive feature of these neuronal corridors is that they
possess similar neurochemical features and connections as
the amygdaloid nuclei, with which they are confluent. The
central and medial amygdaloid nuclei, directly or by way of
the BST, are the major output nuclei of the amygdala (Paré
et al., 2004; Swanson, 2000). The central extended amygdala,
which we will use as a term to include the central amygdaloid
nucleus (CeA) and its corridor to the lateral BST (BSTL), is in-
volved in fear/anxiety and ingestive functions. The medial ex-
tended amygdala, which we will use as a term to include the
medial amygdaloid nucleus (MeA) and its corridor to the me-
dial BST (BSTM), is involved in reproduction and defense
(Alheid and Heimer, 1988; Alheid et al., 1995). We will refer
to the central extended amygdala together with the BSTL as
the central extended amygdala-BSTL complex (or simply cen-
tral extended amygdala complex), and the medial extended
amygdala together with the BSTM as the medial extended
amygdala–BSTM complex (or simply medial extended amyg-
dala complex).
Developmental, neurochemical, hodological and behavior-
al evidence suggests that territories corresponding to the
central and medial extended amygdala–BST complexes of
mammals are present in the avian subpallium as well (Aste
et al., 1998a; Jurkevich et al., 1997, 1999; Roberts et al., 2002; re-
views in Abellán and Medina, 2009; Reiner et al., 2004b; Xie et
al., 2010; Yamamoto et al., 2005). Moreover, both also appear
to be present in amphibian and reptilian subpallia (Martínez-
García et al., 2008; Morona and González, 2008), suggesting
that amygdaloid regions were present in the common tetra-
pod ancestor (Martínez-García et al., 2007). Evidence for cen-
tral and medial extended amygdala–BST complexes in birds
is presented in the following two sections below, with constit-
uents of the central extended amygdala and the BSTL, and
constituents of the medial extended amygdala and BSTM pre-
sented under separate subheadings, respectively.
3.3.1. Central extended amygdala and BSTL
In mammals, neurons of the central extended amygdala are
GABAergic and have descending projections to the lateral hy-
pothalamus, central gray, the parabrachial nucleus and the
nucleus of the solitary tract, which are autonomic centers
that regulate behaviors related to ingestion, fear, and stress/
anxiety (Alheid and Heimer, 1988; Alheid et al., 1995; de
Olmos et al., 2004; Swanson, 2000). GABAergic neurons of the
central extended amygdala projecting to these targets are typ-
ically enriched in any of several neuropeptides, including
corticotropin-releasing hormone (CRH), neurotensin, enkeph-
alin or somatostatin (Alheid et al., 1995; Moga and Gray,
1985; Panguluri et al., 2009; Paré and Smith, 1994; Poulin and
Timofeeva, 2008; Swanson and Petrovich, 1998). Consistent
with its role in autonomic functions, the central extended
amygdala receives input from the posterior intralaminar thal-
amus, the parabrachial nucleus, the nucleus of the solitary
tract, the insular cortex, and the pallial amygdala. It is distinc-
tively rich in calcitonin gene related peptide (CGRP) terminals,
86 BRAIN RESEARCH 1424 (2011) 67–101

representing the parabrachial and posterior intralaminar tha-
lamic input (D'Hanis et al., 2007). The mammalian central
amygdala itself is primarily a striatal derivative (Bupesh et
al., 2011b; García-López et al., 2008; Puelles et al., 2000; Tole
et al., 2005; Waclaw et al., 2010), and recent fate mapping
data indicate that it contains Pax6-expressing cells derived
from dorsal LGE and Islet1-expressing cells derived from
ventral LGE (Bupesh et al., 2011b; Waclaw et al., 2010). Howev-
er, recent evidence also indicates that the medial part of the
central amygdala, and possibly the sublenticular corridor of
the central extended amygdala contain a mixture of neurons
of striatal and pallidal origin (Bupesh et al., 2011b). Pallidal
neurons invading the central amygdala and the corridor con-
tain somatostatin (Bupesh et al., 2011b; García-López et al.,
2008). The BSTL is primarily a pallidal derivative, but some
striatal cells expressing Pax6,Islet1 or Lmo4 invade the BSTL
(Bupesh et al., 2011b; García-López et al., 2008; reviewed in Me-
dina and Abellán, 2009). The central extended amygdaloid
complex in birds includes at least two components: the so-
called subpallial amygdaloid area (SpA; Reiner et al., 2004a;
Roberts et al., 2002; Wild et al., 1990; Yamamoto et al., 2005),
and the BSTL (Abellán and Medina, 2008, 2009; Aste et al.,
1998b; Jurkevich et al., 1999; Reiner et al., 2004b; Roberts et
al., 2002). Both of these were recognized by the Nomenclature
Forum, though not specifically in relationship to an entity
termed the extended central amygdala. The Nomenclature
Forum also did not recognize a central amygdaloid nucleus in
birds. The current understanding of the subdivisions of avian
central extended amygdala and the BSTL are discussed in the
following sections.
3.3.1.1. The subpallial amygdaloid area (SpA) and the central
amygdala. Abellán and Medina (2009) recognized that the
central extended amygdala in chick includes a territory
below the globus pallidus identified by the Nomenclature
Forum as the SpA and a more lateral territory below the cau-
dolateral striatum that the Forum did not recognize. Abellán
and Medina termed these two regions the medial and lateral
parts of the avian extended central amygdala (Fig. 10). They
noted that the medial portion of the central extended amyg-
dala, below the globus pallidus, may correspond to the
sublenticular corridor of the central extended amygdala of
mammals (Reiner et al., 2004a), and include striatal and pallidal
cells (Abellán and Medina, 2009). They proposed that the lateral
portion of the central extended amygdala may correspond to at
least part of the mammalian central amygdala, by the criteria
that it lies directly below the caudolateral striatum and is rich
in striatal, Pax6-expressing (Figs. 10E, F) neurons (Abellán and
Medina, 2009). They additionally recognized a caudolateral ven-
tral part of LSt (which they termed CLSt) as part of the central
extended amygdala as well, and suggested that this also was
part of the avian homologue of mammalian central amygdala
(Figs. 10E, F). Considerable neurochemical and hodological evi-
dence shows a strong similarity between the mammalian sub-
lenticular extended amygdala and the medial part of the avian
central extended amygdala of Abellán and Medina (2009),or
subpallial amygdala (SpA) as the Nomenclature Forum termed
it. As true of mammalian sublenticular central amygdala, neu-
rons of the avian central extended amygdala are GABAergic
(Abellán and Medina, 2009; Yamamoto et al., 2005). Moreover,
many of these neurons are striatal in neurochemistry, contain-
ing the characteristic striatal amygdaloid neuropeptides en-
kephalin, neurotensin and/or corticotropin releasing hormone
(Atoji et al., 1996; Molnar et al., 1994; Reiner et al., 2004a; Richard
et al., 2004; Roberts et al., 2002; Yamamoto et al., 2005). The in-
puts to the medial and lateral portions of the extended central
amygdala of birds also resemble those of the mammalian
Fig. 10 –Major structures comprising the avian central
extended amygdala (EAce) complex, as seen in frontal (A,B) or
oblique-horizontal (C–F) sections showing mRNA expression
of Lmo3 (A,B), SP (C,D) or Pax6 (E,F). Scale bars in A and C =1 mm
(applies to A–F). Expressionof the gene Lmo3 helps to d elineate
the dorsal part of lateral bed nucleus of the stria terminalis
(BSTLd) and part of a lateral corridor that includes the
intrapeduncular nucleus (INP) and the EAce cell corridor,
located below the globus pallidus (GP). The striatal division is
rich in cells expressing substance P (SP) or Pax6, and both
markers are enriched in the striatal (lateral) part of the EAce
complex. In addition, many cells expressing Pax6 or SP also
invade (apparently by tangential migration) the pallidal (more
medial) parts of the EAce complex, including the EAcem and
part of the dorsal BSTL. Refer to list of abbreviations for names
of other structures identified.
From Abellán and Medina (2009).
87BRAIN RESEARCH 1424 (2011) 67–101

central extended amygdala. In both, this regionreceives viscer-
olimbic input from the parabrachial nucleus (Wild et al., 1990),
the nucleus of the solitary tract, and the pallial amygdala
(Atoji et al., 2006; Veenman et al., 1995). Moreover, the avian
central extended amygdala, as well as the CLSt, is enriched in
CGRP terminals, (Lanuza etal., 2000; Reiner et al., 2004b; Roberts
et al., 2002; Yamamoto et al., 2005). Note, however, that neither
the lateral central extended amygdala nor the CLSt in birds is
nearly as rich in CGRP+ fibers as their suggested mammalian
homologue, the central amygdala. As in mammals, the GABAer-
gic/neuropeptidergic neurons of the central extended amygdala
in birds give rise to its outputs, notably to the BSTLand its sub-
nuclei (Fig. 10) and the nucleus of the solitary tract/dorsal vagal
nucleus (Abellán and Medina, 2009; Atoji et al., 2006; Berk, 1987;
Richard et al., 2004; Yamamoto et al., 2005), and may account for
some fibers in those regions containing enkephalin, neuroten-
sin and/or corticotropin releasing hormone. In summary, con-
siderable data support the homology of the medial part of the
avian central extended amygdala (i.e. the subpallial amygdala)
to the mammalian sublenticula r central extended amygdala, in-
cluding the presence of a neurochemically and hodologically
similar region in reptiles (Martínez-García et al., 2008). A homolo-
gy of the lateral part of the avian central extended amygdala
(CLSt) to the mammalian central amygdala also is supported by
considerable data, although differences between these two struc-
tures suggest further study of this issue is needed.
3.3.1.2. Striatal capsule. The intercalated cell masses of the
mammalian amygdala are subpallial neurons interposed be-
tween the central amygdala and the basal complex of the pallial
amygdala and the ventral endopiriform nucleus. The amygda-
loid intercalated cell masses appear to represent an integral
part of the central extended amygdala in mammals, and develop
from the dorsal part of the striatal subdivision of the developing
subpallium, that is the LGE (García-López et al., 2008; Kaoru et al.,
2010; Medina and Abellán, 2009; Waclaw et al., 2010). The amyg-
daloid intercalated cell masses have a GABAergic projection to
the central amygdala and the cholinergic corticopetal cell groups
of the basal telencephalon (including the basal magnocellular
complex), and they are involved in extinction of fear memories
(Paré et al., 2004). A distinctive set of subpallial neurons inter-
posed between the nidopallium and the lateral striatum has re-
cently been termed the avian striatal capsule (Puelles et al.,
2007), and been proposed to be comparable to the intercalated
cell masses of the mammalian amygdala (Abellán and Medina,
2009). Data supporting the proposal include similar develop-
mental origin from the dorsal part of the avian LGE homologue,
some molecular traits, and their position at the border between
the subpallium and what Abellán and Medina (2009) identify as
ventral pallium and thus regard as comparable to mammalian
ventral pallium, including part of the basal amygdalar complex
and the ventral endopiriform nucleus (Figs. 3C–F). The connec-
tions of the avian striatal capsule are unknown and therefore
no hodological support exists at this time. Moreover, the avian
striatal capsule is not juxtaposed to the proposed avian central
amygdala (subpallial amygdalar area), unlike the intercalated
cell masses of the mammalian amygdala.
3.3.1.3. Lateral bed nucleus of the stria terminalis (BSTL). As
noted by the Nomenclature Forum, the BSTL in birds and
mammals is located at the base of the lateral ventricle near
the level of the septopallio-mesencephalic tract and anterior
commissure (Figs. 8C, D). It is characterized by a relative
abundance of neurotensinergic (Atoji et al., 1996; Reiner and
Carraway, 1987; Reiner et al., 2004b), enkephalinergic (Molnar
et al., 1994), and corticotropin-releasing hormone (CRH) neu-
rons (Panzica et al., 1986; Richard et al., 2004), and many calci-
tonin gene related peptide (CGRP; Lanuza et al., 2000) and
noradrenergic fibers (Reiner et al., 1994). In contrast a paucity
of cholinergic cells/fibers (Medina and Reiner, 1994), sparse
dopaminergic terminals (Bailhache and Balthazart, 1993; Reiner
et al., 1994, 2004b), and fewsubstance P-containing neurons and
fibers (Reiner et al., 1983, 2004b) have been reported. Like the
mammalian BSTL (Gray and Magnuson, 1987; Moga et al.,
1989; van der Kooy et al., 1984), the avian BSTL is reciprocally
connected with the hypothalamus, parabrachial nucleus, the
nucleus of the solitary tract, and the dorsal motor nucleus of
the vagus (Arends et al., 1988; Atoji et al., 2006; Bálint et al.,
2011; Berk, 1987; Wild et al., 1990). The BSTL in mammals and
birds, however, appears to be a complex territory with striatal
and pallidal cell subpopulations. In brief, the dorsal and medial
parts of the BSTL in birds and mammals are rich in cells that
develop from a comparable pallidal embryonic subdomain
(Abellán and Medina, 2009; García-López et al., 2008; Xu et al.,
2008), and in birds has been termed the dorsal BSTL by Abellán
and Medina (2009). Lateral to this, in a region termed by them
the dorsolateral BSTL, reside abundant neurons expressing
Pax6/Lmo4 that appear to derive from the striatal progenitor
zone (Figs. 10E, F; Abellán and Medina, 2008, 2009; García-
López et al., 2008; Xu et al., 2008). The BSTL in mammals also
contains a minor subpopulation of Pax6-expressing neurons
derived from dorsal LGE, and an abundant subpopulation of
Islet1-expressing neurons derived from ventral LGE (Bupesh et
al., 2011b). The dorsolateral BSTL of birds is the subdivision
rich in neurons possessing such striatal markers as corticotro-
pin releasing hormone, enkephalin and neurotensin. In adult
birds, however, even the dorsomedial BSTL contains some
enkephalinergic and neurotensinergic neurons, as also true in
mammals (Molnar et al., 1994; Reiner et al., 2004b).The dorsolat-
eral BSTL in birds is confluent with the subpallial amygdala, or
as Abellán and Medina termed it, the medial part of the central
extended amygdala. Note that since thestriatal central extend-
ed amygdala complex projects to the pallidal dorsal BSTL, this
system shows a striato-pallidal organization in birds, as also
noted in mammals (Alheid and Heimer, 1988; Swanson, 2000).
Given that reptiles too possess a BSTL possessing these same
various features, it seems likely that the BSTL is homologous
across amniotes (Martínez-García et al., 2008).
3.3.2. Functional considerations for the central extended
amygdala complex
The central extended amygdala–BSTL in mammals is involved
in food intake and fear/stress behaviors via its connections
with the central parts of the autonomic nervous system
(Luiten et al., 1987; Paré et al., 2004; van der Kooy et al.,
1984). The connections of the avian central extended amygda-
la and BSTL complex with the lateral hypothalamic area, para-
brachial nucleus, nucleus of the solitary tract, and dorsal
motor nucleus of the vagus are consistent with the view that
the homologous circuit in birds is involved with the same
88 BRAIN RESEARCH 1424 (2011) 67–101

basic ingestive and visceral functions (Kuenzel, 1994, 2000;
Kuenzel and Blähser, 1993). In mammals, the central extend-
ed amygdala–BSTL complex projections involving neurons
containing corticotropin-releasing hormone (CRH) are partic-
ularly important for expression of stress and anxiety, and for
regulation of appetite (Clark and Kaiyala, 2003; Gallagher et
al., 2008; Heimer and Alheid, 1991; Krogh et al., 2008). This
peptide is also enriched in the projections of the central ex-
tended amygdala complex in birds and reptiles, particularly
in the BSTL projections (Martínez-García et al., 2008; Richard
et al., 2004), and the CRH+ amygdaloid neurons may thus
play a similar role in non-mammals as mammals (Crespi and
Denver, 2005; Meade andDenbow, 2003; Tachibana et al., 2006).
3.3.3. Medial extended amygdala and BSTM
In mammals, the medial extended amygdala consists of the
medial amygdala itself and a sublenticular neuronal corridor
leading from it to the BSTM. This medial amygdaloid corridor
lies inferior to the sublenticular central extended amygdala
corridor. The medial amygdala receives main olfactory and
vomeronasal input, is rich in neurons with receptors for go-
nadal steroids, and projects to medial preoptic and hypotha-
lamic regions involved in reproduction and defense (Alheid
et al., 1994, 1995; Swanson, 2000). Many of the projections of
the medial amygdala and BSTM are GABAergic (Swanson,
2000; Swanson and Petrovich, 1998), but some are glutamater-
gic (Choi et al., 2005). The complexity of these subpallial cell
groups is further evidenced by the multiple subdivisions de-
scribed for the medial amygdala and BSTM (Alheid et al.,
1995; de Olmos and Heimer, 1999; de Olmos et al., 1985, 2004;
Dong et al., 2001). Recent molecular and fate mapping data
in mouse aid understanding of the developmental basis of
this complexity. The medial amygdaloid nuclear complex
originates primarily from the caudoventral pallidal progenitor
subdivision (MGEcv, also sometimes called the anterior ento-
peduncular area, or AEP) and the commissural preoptic area
(POC) of the subpallium, as confirmed by the numerous
Nkx2.1-lineage neurons in the mature medial amygdala (Xu
et al., 2008) and by recent experimental fate mapping (Bupesh
et al., 2011a). MGEcv-derived neurons in the medial amygdala
can be distinguished from POC-derived neurons because the
former express the transcription factor Lhx6, while the latter
express Shh (García-López et al., 2008). The distribution of
neurons expressing Lhx6 and Shh indicates that MGEcv-
derived and POC-derived cells in mammals are segregated in
the posterior medial amygdala, but intermingled in the anteri-
or medial amygdala (Bupesh et al., 2011a; García-López et al.,
2008). The preoptic origin of part of the medial amygdala has
been confirmed by a fatemap of Dbx1-lineage cells, showing
that most of the nitrergic neurons (co-containing GABA) of
the medial amygdala originate in the preoptic subdivision
(Hirata et al., 2009). In addition, the medial amygdala appears
to include neurons that originate either in ventral pallium
(expressing the transcription factor Lhx9;Bupesh et al., 2011a;
García-López et al., 2008) or the supraopto-paraventricular do-
main (SPV) of the hypothalamus (expressing the transcription
factors Otp and Lhx5;Abellán et al., 2010; Bardet et al., 2008;
Bupesh et al., 2011a; García-Moreno et al., 2010). The ventral
pallial and SPV-derived neurons of medial amygdala are pre-
sumably glutamatergic (Abellán et al., 2010; García-López et
al., 2008), and possibly the source of the glutamatergic projec-
tions of the medial amygdala. The mammalian BSTM also in-
cludes cells derived from MGEcv, POC and extratelencephalic
sources (García-López et al., 2008), including the supraopto-
paraventricular domain (Abellán et al., 2010; Bupesh et al.,
2011a).
The Nomenclature Forum recognized the subpallial part of
nucleus taeniae in birds as a medial amygdala homologue
(Reiner et al., 2004b; Yamamoto et al., 2005). They also noted
the evidence for a BSTM in birds (Aste et al., 1998a; Jurkevich
et al., 1997, 1999; Reiner et al., 2004b; Roberts et al., 2002). In
addition to arginine vasotocin, the BSTM likewise was
shown to contain galanin (Klein et al., 2006). More recently,
Abellán and Medina (2009) termed the subpallial part of nucle-
us taeniae the subpallial medial amygdala (MeAs; Fig. 11).
They suggested that it formed a functional unit with the
BSTM (Fig. 11B) shown as BSTM1 (dorsolateral) and 2 (ventro-
medial) in chicks (Abellán and Medina, 2008, 2009; Jurkevich
et al., 1999), and possibly the ventral part of BSTL (BSTLv,
Fig. 11A; Abellán and Medina, 2008, 2009). A glutamatergic
Fig. 11 –Major structures comprising the avian medial extended amygdala (EAme) complex, as seen in frontal sections
showing mRNA expression of the transcription factor Lhx6. These structures include the subpallial medial amygdala (MeAs)
and the BSTM (which show two subdivisions in chicken, called BSTM1 and BSTM2). Scale bar =1 mm. Note the expression of
Lhx6 in other pallidal structures of the telencephalon, including the globus pallidus (GP), the BSTLd and the medial EACe. Refer
to list of abbreviations for names of other structures identified.
Modified from Abellán and Medina (2009).
89BRAIN RESEARCH 1424 (2011) 67–101

population of neurons has been identified in the avian medial
amygdala (Abellán and Medina, 2008, 2009; Abellán et al.,
2009; Bardet et al., 2008; Puelles et al., 2007), which include
neurons derived from the ventral pallium, and Otp-expressing
neurons of supraopto paraventricular origin. Additionally, a
sub-nucleus termed the amygdaloid taenial nucleus (ATn
shown in Fig. 17 of Puelles et al., 2007) has been identified in
chickens located dorsal and medial to the MeAs (Fig. 11 and
last cross-sectional plate of Fig. 1) suggesting that the avian
medial amygdala (MeAs) may comprise more than the tradi-
tional nucleus taeniae.
A medial amygdala and BSTM have also been described in
reptiles and amphibians (Martínez-García et al., 2008; Morona
and González, 2008), suggesting that a medial amygdala–
BSTM corridor was present in the forebrain of the common
tetrapod ancestor.
3.3.3.1. Subpallial medial amygdala. In chickens, the subpal-
lial medial amygdala (called the subpallial amygdaloid nucleus
of the taeniae by the Nomenclature Forum) includes inter-
mingled neurons derived from pallidal/MGEcv and preoptic pro-
genitor zone subdivisions (expressing Lhx6 and Shh, respectively),
resembling in this respect the anterior subnucleus of the medial
amygdala of mammals (Abellán and Medina, 2009). Moreover,
the subpallial medial amygdala of birds (Fig. 11)contains
GABAergic neurons (Abellán and Medina, 2009; Sun et al., 2005;
Yamamoto et al., 2005) and nitrergic neurons (Balthazart et al.,
2003; Panzica et al., 1994), resembling the finding of GABAergic
and nitrergic neurons in the mammalian medial amygdala
(Swanson, 2000; Tanaka et al., 1997). In addition, the avian sub-
pallial medial amygdala receives olfactory input from the main
olfactory bulb (Reiner and Karten, 1985) and piriform cortex
(Bingman et al., 1994; Veenman et al., 1995), and projects to the
BST complex and medial preoptic region (Balthazart and Absil,
1997; Cheng et al., 1999). As true of the mamma lian medial amyg-
dala, the avian subpallial medial amygdala is reciprocally con-
nected with the hippocampal formation (Atoji and Wild, 2004;
Atoji et al., 2002). Importantly, the avian subpallial medial amyg-
dala is enriched in sex-steroid concentrating neurons possessing
estrogen and androgen receptors and the enzyme aromatase
(Balthazart et al., 1998; Foidart et al., 1999; Martinez-Vargas et
al., 1978). Their abundance is more striking in males (Watson
and Adkins-Regan, 1989), and reflects the role of the steroid re-
ceptors and the neurons that contain them in male sexual
behavior (Absil et al., 2002; Panzica et al., 1996; Thompson et
al., 1998). In summary, data in birds, reptiles and amphibians
(Martínez-García et al., 2008; Morona and González, 2008)
stronglysupport the homologyof avian subpallialmedial amyg-
dala and the medial amygdala of mammals, particularly its an-
terior subnucleus. A distinct sublenticular corridor from the
avian medial amygdala to the BSTM has not, however, been
clearly delineated.
3.3.3.2. Medial bed nucleus of the stria terminalis (BSTM). The
BSTM of chicken also includes neurons of pallidal/MGEcv
and preoptic origins, thus resembling the BSTM of mammals
(Abellán and Medina, 2008, 2009). In quail, a single BSTM nucle-
us has been documented by neurochemical criteria (Aste et al.,
1998a), while in chickens BSTM has been shown to consist of
two subnuclei (Fig. 11B), as evidenced by immunocytochemistry
and in situ hybridization histochemistry (Jurkevich et al., 1999).
The two BSTM nuclei of chickens were termed the BSTMdl and
BSTMvm by Jurkevich et al. (1999), and adopted as the BSTM1
and BSTM2, respectively, by the Nomenclature Forum (Reiner
et al., 2004b). Similar to the mammalian BSTM, steroid-
responsive neurons of the avian BSTM include cells containing
aromatase (Aste et al., 1998b; Balthazart et al., 1990; Roselli,
1991; Shinoda et al., 1994; Xie et al., 2011), and cells containing
vasotocin (Aste et al., 1998b; De Vries et al., 1994; Jurkevich et
al., 1999; Kiss et al., 1987; Viglietti-Panzica et al., 1992; Xie et al.,
2011). As also true of mammalian BSTM, the avian BSTM (and
potentially the embryologically-related ventral part of BSTL) re-
ceives olfactory input from the piriform cortex (Bingman et al.,
1994; Veenman et al., 1995), and possibly the subpallial medial
amygdala (Balthazart and Absil, 1997), and projects to the medi-
al preoptic nucleus and medial hypothalamus, which are in-
volved in male mating behavior (Absil et al., 2001, 2002; Xie et
al., 2010). In Japanese quail, AVT neurons of the BSTM are the
projection neurons targeting the POM and hypothalamus
(Absil et al., 2002) and some of their axons also reach the subpal-
lial medial amygdala (Balthazart and Absil, 1997).
3.3.4 Functional considerations for subpallial medial
amygdala and BSTM
In mammals, the medial extended amygdala–BSTM complex
plays a key role in mating, sexual, defensive, and aggressive be-
haviors, for which olfactory information to the medial amygda-
la is extremely important (Choi et al., 2005; Swanson, 2000). In
birds, the hodological and behavioral data indicate that the me-
dial amygdala and BSTM play a similar role (Absil et al., 2002;
Panzica et al., 1998; Thompson et al., 1998; Xie et al., 2010). Al-
though birds are relatively microsmatic, electrophysiological re-
sponses in the avian olfactory bulb to odorants are comparable
to those in mammals (McKeegan, 2002), and olfactory cues are
used by birds in social and sexual interactions (Caro and Baltha-
zart, 2010). The medial amygdala and BSTM, which receive ol-
factory information (Bingman et al., 1994; Veenman et al.,
1995), are involved in olfactory-related behaviors (Balthazart
and Schoffeniels, 1979). Numerous studies directly demonstrate
the role of the avian subpallial medial amygdala and BSTM in
reproductive behavior. For example BSTM1 and BSTM2 are sig-
nificantly larger in males, are steroid-responsive, and play a
role in male copulatory behavior (Aste et al., 1998b; Del Abril et
al., 1987; Guillamón and Segovia, 1997; Jurkevich et al., 1999;
Kiss et al., 1987; Panzica et al., 1998; Viglietti-Panzica et al.,
1992; Voorhuis et al., 1988). The avian BSTM2 is involved specif-
ically in male appetitive sexual behavior (Xie et al., 2010, 2011).
Arginine vasotocin (AVT) is the non-mammalian homologue
of vasopressin (Acher et al., 1993), and castration inquail elimi-
nates AVT-expressing neurons and decreases the number of
aromatase-expressing neurons in the BSTM and medial preop-
tic hypothalamus (Aste et al., 1998b; Panzica et al., 1999).
3.4. Basal telencephalic cholinergic and non-cholinergic
corticopetal system
In mammals, the basal telencephalic corticopetal system con-
sists of large cholinergic neurons dispersed over the pallidal-
substantia innominata region, the medial septum-diagonal
band nucleus, and the magnocellular preoptic nucleus (Gritti
90 BRAIN RESEARCH 1424 (2011) 67–101

et al., 1993, 2003). These cells partly overlap the globus pallidus
and ventral pallidum of the basal ganglia and the extended
amygdala inthe so-called substantia innominata, but they rep-
resent functionally distinct neurons that typically project to cor-
tical regions. The cholinergic corticopetal projections are in
contrast to the major descending GABAergic projections typical
of the basal ganglia and BST-extended amygdala systems
(Alheid et al., 1995; Gritti et al., 1997). Corticopetal cholinergic
neurons play an important role in modulation of cortical activi-
ty, and in attentional and arousal processes (Záborszky et al.,
1999) that affect learning and memory (Cape and Jones, 2000;
Cape et al., 2000; Metherate et al., 1988, 1992). Similarly, the
avian corticopetal system consists of scattered large cholinergic
neurons that are dispersed over the pallidum-substantia inno-
minata, and septal-diagonal band regions (Medina and Reiner,
1994; Medina et al., 1995). In birds, telencephalic structures
containing cholinergic neurons (Reiner et al., 2004b)include
the basal magnocellular nucleus (NBM, Figs. 11Aand12), nucle-
us of the diagonal band, horizontal limb (NDBh, Figs. 11A
and 12A), nucleus of the diagonal band, vertical limb (NDBv,
Fig. 12B) and commissural nucleus of the septum (CoS, Fig. 11A).
3.4.1. Nucleus basalis magnocellularis
Cholinergic cells of nucleus basalis magnocellularis (NBM) in
birds take residence primarily in and about the lateral and medi-
al forebrain bundle but also dispersed in the globus pallidus,
ventral pallidum and intrapeduncular nucleus (Medina and Rei-
ner, 1994; Reiner et al., 2004b). This field of cholinergic neurons
thus overlaps GABAergic neurons in each region. The choliner-
gic neurons of the avian NBM (Figs. 11Aand12) are comparable
to those in the mammalian nucleus basalis of Meynert, which
overlaps the globus pallidus, ventral pallidum and substantia
innominata. Perikarya of the basal forebrain cholinergic system
of mammals projecttopographically to pallial and cortical areas,
including hippocampus, neocortex, and pallial amygdala
(Záborszky et al., 1999). Various pallial regions in birds also re-
ceive cholinergic innervation, including rostromedial nidopal-
lium, temporo-parieto-occipital area (TPO), hippocampal
complex and dorsal arcopallium (Medina and Reiner, 1994).
Tract-tracing and double-labeling data indicate that cholinergic
neurons of thebasal forebrain in birdsproject to the pallium in a
roughly topographic manner (Bagnoli et al., 1992; Krebs et al.,
1991; Medina et al., 1995). Since the intrapeduncular nucleus is
rich in cholinergic neuronsand projects to the TPO, its choliner-
gic neurons appear to be part of the NBM systemin birds (Brauth
et al., 1978). The cholinergic innervation of the pallium in birds
and mammalsis associated with their enrichment in muscarin-
ic cholinergic receptors (Brann et al., 1988; Dietl et al., 1988; Koh-
ler et al., 1995; Wächtler and Ebinger, 1989). In mammals, the
basal forebrain cholinergic corticopetal cell fields receive input
from the pallial amygdala, and the central and intercalated nu-
clei of the subpallial amygdala (Grove, 1988; Paré and Smith,
1994; Price and Amaral, 1981; Russchen, 1982; Russchen et al.,
1985a,b), and the brainstem reticular formation, including the
pedunculopontine nucleus (Datta and Prutzman, 2005; Pal and
Mallick, 2004). In birds, it appears that the region of the NBM
cholinergic neurons receives input from limbic striatum (in-
cluding nucleus accumbens) and from the arcopallium–amyg-
daloid complex (Medina and Reiner, 1997; Veenman et al.,
1995). Tract-tracing data also suggest that the NBM receives
input from a rostral rhombencephalic tegmental region (Kitt
and Brauth, 1986b) that contains the pedunculopontine nucle-
us. Thus, inputs, outputs, and neurochemistry of the NBM in
birds closely resemble those in mammals.
3.4.2. Nucleus of the diagonal band
Cholinergic neurons in the diagonal band and ventromedial
septum are also part of the mammalian basal forebrain cho-
linergic system (Woolf, 1991). Cholinergic neurons of the nu-
cleus of the diagonal band (NDB) occur as far caudally as the
nucleus of the septal commissure. Neurons from the vertical
limb of the diagonal band and medial septum provide major
cholinergic innervation of the hippocampus while those of
the horizontal limb of the diagonal band project to the olfacto-
ry bulbs. Similarly, the avian NDB (Figs. 11A and 12B) projects
heavily into the hippocampal and parahippocampal areas
(Atoji et al., 2002; Benowitz and Karten, 1976; Casini et al.,
1986; Montagnese et al., 2004). Tract-tracing and double-
Fig. 12 –Major structures of the cholinergic corticopetal system seen with markers of ChAT (mRNA or protein), which label
cholinergic cells. A. Nucleus basalis magnocellularis (NBM). B. Nucleus of the diagonal band (NDB). C. Higher magnification of
the NBM of Fig. 12A showing more detail of ChAT expression in NBM, GP and low expression in LSt. Scale bars in A and
B= 1 mm.
Modified from Abellán and Medina (2009).
91BRAIN RESEARCH 1424 (2011) 67–101

labeling data indicate that cholinergic neurons of the NDB are
at least partly the source of this projection to the hippocampal
complex, as well as to medial pallial territories of the Wulst
and dorsal ventricular ridge (Medina et al., 1995).
3.4.3. Nucleus commissuralis septi (Commissural septal
nucleus)
The avian commissural septal nucleus (CoS) can be observed
just dorsal to the anterior commissure and lateral to the nu-
cleus of the hippocampal commissure (Fig. 11). The nucleus
projects heavily to the hippocampal and parahippocampal
areas (Atoji et al., 2002; Benowitz and Karten, 1976; Casini et
al., 1986; Montagnese et al., 2004). In general, its inputs resem-
ble those to the NBM and NDB.
3.4.4. Functional considerations for corticopetal system
The basal forebrain system has been implicated in cortical
learning and memory in mammals (Záborszky et al., 1999),
and there is a strong correlation between the loss of choliner-
gic neurons and the loss of memory (Auld et al., 2002). Little is
known, however, about the role of these cholinergic neurons
in learning and memory in birds. The similarities between
mammals and birds in the inputs, outputs, and neurochemis-
try of this system of cholinergic neurons suggest that they
likely play a key role in learning and memory in birds as
well. Pharmacological blockade of muscarinic cholinergic re-
ceptors, in fact, has been shown to impair learning and mem-
ory in diverse avian species (Kohler et al., 1996; Mineau et al.,
1994; Patterson et al., 1990; Savage et al., 1994; Zhao et al.,
1997). Moreover, beta-amyloid toxicity, which is known to
damage the basal forebrain cholinergic system in mammals,
is known to impair memory in chicks (Gibbs et al., 2010).
4. Conclusions
The present goal was to provide current developmental, hodo-
logical, chemoarchitectonic and behavioral/functional data
that further refine understanding of the avian subpallium and
its relationship to that in mammals. We have organized the
cell groups of the lateral wall of the avian subpallium into four
distinct neural systems, and pointed out similarities and differ-
ences between mammals and birds in the constituent parts of
these systems. Noteworthy similarities that had not been previ-
ously recognized are apparent, as well as some differences that
advance understanding of the evolution and function of the
avian subpallium. A subsequent paper will address septal struc-
tures residing in the medial subpallial wall that comprise a fifth
neural system in the avian subpallium.
Acknowledgments
We wish to thank Lauren Kuenzel for her excellent technical
assistance for completing Fig. 1 and sizing, grouping and pro-
viding the appropriate magnification bars for some of the
photomicrographs presented in the paper. We also thank
Dr. Antonio Abellán for providing some of the images utilizing
in situ hybridization histochemistry. Supported in part by NSF
Grant # IOS-0842937 and Competitive USDA/AFRI/NIFA Grant
no. 2005-35203-15850 to W.J.K., NIH Grant # NS-19620, NS-28711
and NS-57722 to A.R., Grant OTKAT73219 (Hungary) to A.C.,
Spanish Ministry of Science and Innovation-FEDER Grant no.
BFU2009-07212/BFI to L.M. and NIH Grant RO1 MH066128 to D.P.
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