Tracing the human brain's classical language areas in extant and extinct hominids

Abstract

Language is a cognition that makes us human. It is a function of the structure of the human brain that is made possible by complex wiring of neural networks that evolved over millions of years since humans shared the last common ancestor with the great apes. The human brain accommodates two principle cortical areas that are strongly involved in computing linguistic processes: Broca's and Wernicke's areas. Discovered in the latter half of the 19th century, the regions represent localized but relatively segregated linguistic modules which are linked through connective pathways. Broca's and Wernicke's areas are ancient parts of the primate brain, however, their functional specializations have undergone significant transformations during primate evolution. This chapter will review neurobiological findings concerning the internal make-up and function of the homologous brain areas to Broca's and Wernicke's areas in extant nonhuman primates and discuss relevant knowledge that exists on the brain morphology of extinct hominins. Comparative neurobiology holds the key to understanding how the core language areas have developed their specialized functions in human brains by offering insights into developments that could have been the driving forces for language during evolutionary history.

Full text

29
1
Tracing the human brain's classical
language areas in extant and extinct
hominids
Eva Maria Luef
Seoul National University, College of Education
Abstract Language is a cognition that makes us human. It is a function of the
structure of the human brain that is made possible by complex wiring of neural
networks that evolved over millions of years since humans shared the last com-
mon ancestor with the great apes. The human brain accommodates two principle
cortical areas that are strongly involved in computing linguistic processes: Broca's
and Wernicke's areas. Discovered in the latter half of the 19th century, the regions
represent localized but relatively segregated linguistic modules which are linked
through connective pathways. Broca's and Wernicke's areas are ancient parts of
the primate brain, however, their functional specializations have undergone sig-
nificant transformations during primate evolution. This chapter will review neu-
robiological findings concerning the internal make-up and function of the homol-
ogous brain areas to Broca's and Wernicke's areas in extant nonhuman primates
and discuss relevant knowledge that exists on the brain morphology of extinct
hominins. Comparative neurobiology holds the key to understanding how the
core language areas have developed their specialized functions in human brains

Eva Maria Luef
30
by oering insights into developments could have been the driving forces for lan-
guage during evolutionary history.
Keywords brain, Broca's area, classical language areas, evolution, origins,
Wernicke's area
1 INTRODUCTION
From so simple a beginning, endless forms most
beautiful and most wonderful have been,
and are being, evolved.
— Darwin, 1859
Throughout history, many societies believed that language was a gift
from God to humans. According to the Bible, immediately upon creation
Adam received the task from God to give names to all living things and
hence develop a language with which he could communicate with Eve.
Human society and language are treated as inseparable entities not just
by the authors of the Bible, but even more so by modern science that has
demonstrated how deeply ingrained language is into our biological and
social existence. Contrary to biblical belief, this close relationship is a
result of the evolutionary pressures of the ancestral past moulding and
shaping the unique human mind as we know it today.
Language is a multifaceted cognitive ability dependent on a complex
brain to support it. For humans, communication requires a wide range of
dierent cerebral processes contributing to construct linguistic mean-
ing in the brain. The essence of the neurobiology of language consists
of identifying particular linguistic functions and their cerebral control
centers to be able to assign functions to specific brain areas. Many con-
temporary language-brain models are deeply rooted in the premise that
two cortical left-hemispheric areas govern the majority of language
processes (Price, 2012). This is not to say that no other cerebral regions
contribute to linguistic tasks or that the core language areas exclusively
compute language. A variety of subcortical structures may be involved
in lexical, phonological, syntactic, and/or semantic processes (e.g., Du

Tracing the human brain's language areas
31
& Brown-Schmidt, 2017; Duau, Moritz-Gasser, & Mandonnet, 2014;
Tiedt et al., 2017). In addition, right-hemispheric structures also make
important contributions to language (Silbert, Honey, Simony, Poeppel, &
Hasson, 2014). More generally, linguistic processing can build upon and
benefit from non-linguistic cognition, such as numerical or spatial pro-
cessing (see, e.g., de Bruin, Roelofs, Dijkstra, & Fitzpatrick, 2014; Hauser,
Chomsky, & Fitch, 2002), which makes the definition of what constitutes
a language area dicult. The two core language areas, namely Broca's
and Wernicke's areas, are historically important and well-researched
brain regions in terms of linguistic cognition, and a considerable body of
research has consolidated their undebated role for language.
This review will discuss the evolutionary development of the core
language areas of modern human brains as we know them today. Starting
with an historical overview of their discoveries and important findings
from early brain-language research of the 19th century, it will continue
with a description of which cytoarchitectonic studies have contribut-
ed to our current knowledge of the language areas and their functions.
Neurobiological studies on nonhuman primates will show how equiva-
lent brain regions in monkeys and apes process information related to
species-specific communication and how functionality of those areas
changed during the evolution of Homo sapiens. Lastly, archaic humans
– extinct members of the genus Homo – which are considered as evolu-
tionary intermediaries between the great apes and humans, will be the
focus of discussion. Evidence relating to the existence of the core lan-
guage areas in the brains of various species of extinct hominins can pro-
vide compelling insights into the evolutionary history of neurolinguistic
structures of the human brain.
2 THE HUMAN CORE LANGUAGE AREAS
The neurobiological basis of language has traditionally been considered
as centered upon two core language areas called Broca's area and Wer-
nicke's area. They are named after their discoverers, the French phy-
sician Pierre Paul Broca (1824–1880) and the German neurologist Carl

Eva Maria Luef
32
Wernicke (1848–1905), who were among the first to describe their role
in linguistic processing.
Examining two patients who were unable to speak, Broca discovered
that damage to the left inferior frontal gyrus of the cerebral cortex led
to language production deficits (so-called Broca's aphasia or non-fluent
aphasia, see Broca, 1861, 1865). Neither claims of location nor left-later-
alization of this brain area were entirely new (for a review of the histor-
ical debate over the discovery of the lateralized language area known as
Broca's area see, e.g., Finger, 2010). However, previous work was rather
preliminary and lacking in many of the evidential details that were lat-
er provided by Broca, who has thus historically been credited with the
discovery of that language area (Cubelli & Montagna, 1994). Tradition-
ally, Broca's area has been described as a productive region concerned
with the encoding of vocal signals into meaningful syllables, words (e.g.,
Indefrey & Levelt, 2004; Papoutsi et al., 2009) and sentences (Embick,
Marantz, Miyashita, O'Neil, & Sakai, 2000).
Post-mortem analyses of the brains of both Broca's patients and re-
cent re-examinations with modern neuroimaging techniques revealed
their lesions to be more extensive than solely to the posterior part of the
left inferior frontal gyrus. They include the insula, anterior parts of the
superior temporal lobe and parts of the inferior parietal lobule as well
as subcortical parts, such as the claustrum, putamen and globus pal-
lidus (Cabanis, Iba-Zizen, Abelanet, Monod-Broca, & Signoret, 1994;
Castaigne, Lhermitte, Signoret, & Abelanet, 1980; Dronkers, Plaisant,
Iba-Zizen, & Cabanis, 2007). Based on these findings, it has become clear
in the last few decades that the clinical description of Broca's aphasia
also involves substantial subcortical and insular damage (Petrides, 2014)
and that a localized lesion to solely Broca's area results in a rather mild
and reversible language production problem (Mohr et al., 1978; Penfield
& Roberts, 1959).
In 1874, Carl Wernicke identified another cortical area whose dam-
age led to language impairment, in this case in the domain of language
perception. Disruptions to the posterior portion of the left superior tem-
poral gyrus result in a type of aphasia, which is primarily characterized
by poor speech/language comprehension but relatively fluent language
output (so-called Wernicke's aphasia or fluent aphasia, see, e.g., Benson
& Ardila, 1996). Wernicke's area is most commonly described as a recep-

Tracing the human brain's language areas
33
tive region for processing and integrating auditory sensory information
(Guenther, 2016) and lies immediately posterior to the primary audito-
ry cortex, which is considered crucial for the perceptual processing of
speech (Petrides, 2014). Wernicke (1881) suggested that the critical re-
gion for auditory language comprehension spans the superior temporal
gyrus, including the cortex of the superior temporal sulcus and the ad-
jacent lip of the middle temporal gyrus. He proposed the existence of
a larger peri-Sylvian cortical and insular language region in the human
brain, including the core language region identified by him. This postu-
lation proved remarkably consistent with the findings of the majority
of studies that would follow within the next century, including neuro-
psychological as well as modern functional neuroimaging studies (e.g.,
Dronkers, Redfern, & Ludy, 1995; Friederici, 2011; Penfield & Roberts,
1959).
Typical language processing in the human brain is relatively strictly
lateralized. Broca's and Wernicke's areas, as well as Heschl's gyrus and
the insula, are primarily left-hemispheric regions (Bidula & Króliczak,
2015; but see Keller et al., 2011), whereas a number of right-hemispheric
brain regions also play a role, such as the mid part of the superior tempo-
ral sulcus (Glasel et al., 2011; Leroy et al., 2015).
After the discoveries of Broca and Wernicke, the German physician
Ludwig Lichtheim developed a model of language function that placed
both core language areas at the center and attempted to describe how
they interact for linguistic computing (Graves, 1997; Lichtheim, 1885).
Broca's view of brain language processes corresponded with a mosaic
map of specific and separate language function centers, including a gen-
eral faculty for languages and a specific faculty of articulation and dier-
ent input/output pathways (peripheral sensory, motor nerve), between
which no connection was described (Broca, 1865). Wernicke, on the oth-
er hand, drawing upon his teacher and mentor Theodor Meynert, pro-
posed connective pathways between dierent language centers and saw
all linguistic functions as inter-related in both functional and anatomical
terms (Wernicke, 1874, 1881). Based on Wernicke's paradigm, Lichtheim
formulated the Wernicke-Lichtheim Model of linguistic processing (later
modified most notably by Geschwind, 1965) which defines Wernicke's
area as the auditory center, Broca's area as the motor output center,
and both connected to an (non-localized) conceptual center (Lichtheim,

Eva Maria Luef
34
1885). The model puts strong emphasis on the functional connectivity of
cerebral areas and their associative networks, a view that was support-
ed by other researchers at the time who showed fiber tracts linking the
core language areas (e.g., Burdach, 1822; Dejerine, 1895). Thanks to the
pioneering work by Geschwind (1970), a large fiber tract between Broca's
and Wernicke's area, the arcuate fasciculus, was identified as a crucial
pathway for language processing (see also Marin in this volume). Later
research identified additional fiber tracts linking lateral areas of the tem-
poral cortex with the frontal cortex (Petrides & Pandya, 1988; Schmah-
mann et al., 2007), and a part of the superior longitudinal fasciculus was
described as most crucial for language processing (e.g., Schmahmann et
al., 2007). In the last ten to fifteen years, numerous studies using diu-
sion tensor imaging (DTI-tractography) have delineated with modern
neuroimaging techniques the relationship of language to white matter
pathways, such as the arcuate fasciculus, ventral pathway and uncinate
fasciculus (Catani & Jones, 2005; Frey, Campbell, Pike, & Petrides, 2008;
Saur et al., 2008). Whether the arcuate fasciculus actually plays the role
in linguistic processing that Geschwind described has been debated re-
cently (see Dick & Tremblay, 2012, for a review).
Undoubtedly, most researchers agree with the general premise of
the dual-pathway model of language/speech processing, where a dorsal
stream maps auditory speech sounds to articulation and a ventral stream
maps auditory speech sounds to meaning (Ungerleider & Haxby, 1994);
however, the exact neural connections comprising the system are often
considered controversial (Hickok, 2009; Rauschecker, 2011; Rauscheck-
er & Tian, 2000; Saur et al., 2008; Weiller, Bormann, Saur, Musso, & Ri-
jntjes, 2011). Although the extensive degree of connections between the
dierent brain language areas was not known at the end of the 19th cen-
tury, Wernicke's and Lichtheim's work guided future researchers in the
direction that proved to be most useful for finding the neurobiological
foundations of language. The Wernicke-Lichtheim Model came to be the
standard neuropsychological model for language and was elaborated on
extensively over the following 100 years (Ben Shalom & Poeppel, 2008;
Graves, 1997), spawning many modern descendants (see, e.g., Friederici,
2002; Hickok & Poeppel, 2004; Indefrey & Levelt, 2004; Price, 2000).
Broca's and Wernicke's areas are often inconsistently defined in the
literature as both involving large portions of the cortex with relatively

Tracing the human brain's language areas
35
vague boundary markings (Guenther, 2016). In general, there is substan-
tial variation concerning the precise boundaries of the areas among indi-
viduals as well as between hemispheres of the same individual (Amuts et
al., 1999; Steinmetz & Seitz, 1991). One way to delineate discrete cortical
areas more narrowly is to define them on the basis of their cellular or-
ganization (i.e., the cytoarchitecture). Cells receive, compute and send
out information to other cortical and subcortical structures with which
they are linked (Petrides, 2014), and their internal make-up is relevant
to understanding their particular functions. The procedure of hardening
brains to stain cellular elements of thinly sectioned slices only became
possible in the latter part of the 19th century and was pioneered by Carl
Wernicke's teacher Theodor Meynert, who was able to demonstrate dif-
ferent cell types and various layers of neurons in dierent cortical re-
gions (Meynert, 1867). His work was followed by other researchers, in-
cluding the German neuro-anatomist Korbinian Brodmann who in 1909
published the most famous cytoarchitectonic map of the human cerebral
cortex, introducing the numerical nomenclature to denote the cortical
regions that is still widely used today (i.e., “Brodman area” or “BA” plus
corresponding number of his cytoarchitectonic map). The following two
centuries saw a rise in interest in cytoarchitecture due to the develop-
ment of new methods and techniques (e.g., Economo & Koskinas, 1925;
Sarkissov, Filimono, Kononowa, Preobraschenskaja, & Kukuew, 1955),
and beginning in the 1980s, functional neuroimaging of distinct foci of
functional activity in the human brain drew on cytoarchitecture to define
cortical regions (e.g., Talairach & Tournoux, 1988).
Both Broca's and Wernicke's areas correspond to more than one
Brodmann area. Broca's area includes Brodmann's areas 44 and 45, with
area 44 lying on the pars opercularis and area 45 on the pars triangularis
of the inferior frontal gyrus (Amuts et al., 2010), while Wernicke's area
corresponds to parts of Brodmann's areas 21, 22 (central and posterior
superior temporal gyrus), 41 and/or 42 (Ardila, Bernal, & Rosselli, 2016).
Even though there are no exact correspondences between the core lan-
guage areas and their cytoarchitecture, the cytoarchitectonic divisions of
the human cortex are particularly useful in cross-species comparisons.
Cortical cells, like all other biological structures, change slowly and thus
remain highly conserved for a longer evolutionary period (Geschwind &

Eva Maria Luef
36
Rakic, 2013), opening up the possibility of comparative neurobiological
studies across related species.
3 HOMOLOGUES OF BROCA'S AND WERNICKE'S AREAS IN
NONHUMAN PRIMATES
Primates first appeared in the fossil record around 55 million years ago
(Seiert, Perry, Simons, & Boyer, 2009), with the evolutionary lineage
leading to modern humans splitting from the great ape lineage about
seven to eight million years ago (Langergraber et al., 2012). The diverse
order of primates includes prosimians, such as lemurs and tarsiers, and
a multitude of simian species, for instance marmosets, capuchins, ma-
caques and apes. The great apes (Hominidae) are the closest living rel-
atives of humans and share over 97% of genes with them (Locke et al.,
2011). Macaque monkeys are, after humans, the most widespread pri-
mate genus and share about 93% of their genes with humans (Gibbs et
al., 2007). Research pertaining to the evolution of human behavior is of-
ten focused on chimpanzees, but neuroscience widely uses macaques to
model functions of the human brain.
During human evolution, there was substantial neurological rewiring
and reorganization of the cortex, wherein some areas increased in size
(e.g., the anterior prefrontal cortex) while others decreased (e.g., parts
of the insular cortex, see Semendeferi, Armstrong, Schleicher, Zilles, &
Van Hoesen, 1998, 2001). The increase in white matter volume of the pre-
central cortex indicates that the frontal lobes in humans have increased
in neurological complexity as compared to those in great apes (Schoen-
emann, Sheehan, & Glotzer, 2005). The human brain is not just an en-
larged version of the chimpanzee brain but diers with regard to form
and function (Rilling, 2006).
Cytoarchitectonic studies have helped trace the nonhuman origins
of specific human brain regions to draw conclusions as to their evolu-
tionary development. Cortical regions homologous (in cell make-up) to
Broca's and Wernicke's areas have been identified in macaque monkeys
(Galaburda & Pandya, 1982; Preuss, 2000) as well as in all great apes
(Cantalupo & Hopkins, 2001; Spocter et al., 2010), and those areas seem

Tracing the human brain's language areas
37
to be involved specifically in the processing of species-specific vocal and
gestural communication signals (Gil-da-Costa et al., 2006; Petrides, Ca-
doret, & Mackey, 2005; Taglialatela, Russell, Schaeer, & Hopkins, 2008).
The function of Broca's area in humans may thus be a specialization of
more ancient brain functions related to vocal and gestural communica-
tion in Old World primates (Schenker et al., 2010).
The macaque homologue of Broca's area has gained fame with the
discovery of mirror neurons, which are a class of neurons that represent
meanings of actions (in the sense of an action vocabulary) accessible
through auditory stimuli (Kohler et al., 2002). Therefore, the link be-
tween motor action and speech is not new to the human Broca's area but
has an evolutionary precedent, a fact that has fed various hypotheses on
language origins (e.g., Gallese, 2008).
While Broca's area is lateralized to the left cortical hemisphere in
most humans (Toga & Thompson, 2003), the degree of lateralization of
homologous regions in nonhuman primates is still unclear. Allometric
measurements of the homologue of Broca's area in chimpanzees are not
in agreement over hemispheric specialization (Cantalupo & Hopkins,
2001; Schenker et al., 2010). Human brains are characterized by the so-
called Broca's cap, a bulge at the level of the temporal pole that includes a
part of Broca's area, namely Brodmann area 45 (see Falk, 2014). A similar
structure in chimpanzees, called the orbital cap (which does not exact-
ly correspond to Broca's cap, see Falk, 2014), may or may not show size
dierence between the two hemispheres (Cantalupo & Hopkins, 2001;
Schenker et al., 2010; Sherwood, Broadfield, Holloway, Gannon, & Hof,
2003). Nevertheless, behavioral studies suggest a certain degree of lat-
eralization of communicative functions in nonhuman primates (Vau-
clair, 2004). Chimpanzees have been shown to possess a tendency to
process species-specific sounds primarily in the inferior frontal gyrus of
the left hemisphere (Taglialatela et al., 2008; Wilson & Petkov, 2011). In
macaques, stimulation of the left Broca's area homologue elicits orofa-
cial movements (Petrides et al., 2005), and orofacial asymmetries were
shown to be associated with the production of species-specific calls in
marmosets, macaques and chimpanzees (Fernández-Carriba, Loeches,
Morcillo, & Hopkins, 2002; Hook-Costigan & Roger, 1998; Schenker et
al., 2010). Due to the fact that chimpanzees tend to produce asymmetric
orofacial movements during the production of (learned) calls, it has been

Eva Maria Luef
38
suggested that both tasks are functionally lateralized to the left hemi-
sphere (Losin, Russell, Freeman, Meguerditchian, & Hopkins, 2008).
While lateralization of the nonhuman homologue to Broca's area
is still contested, more agreement exists concerning asymmetry in the
chimpanzee homologue of Wernicke's area (Hopkins et al., 2016; Spocter
et al., 2010). In humans, the planum temporale at the core of Wernicke's
area is significantly enlarged in the left hemisphere, with the left-hemi-
spheric area being approximately ten times larger in size than the right
one (Geschwind & Levitsky, 1968). The nonhuman homologue area of
Brodmann area 22, comprising the largest part of Wernicke's area, is
called the temporo-parietal area (Tpt) and has been localized in ma-
caques, galagos (Gannon, Kheck, & Hof, 2008; Preuss & Goldman-Rakic,
1991) and all great apes (Hopkins, Marino, Rilling, & MacGregor, 1998,
see Figure 1). The human-like lateral asymmetry is already evident in ba-
boons and great apes (Hopkins et al., 1998; Hopkins & Nir, 2011; Marie et
al., 2017), indicating that the planum temporale asymmetry dates back to
a common ancestor of catarrhine primates (Sherwood, Subiaul, & Zaw-
idzki, 2008).
A number of behavioral studies suggested that perception of spe-
cies-specific vocalization may be lateralized to the left cerebral hemi-
sphere in macaques (e.g., Ghazanfar, Smith-Rohrberg, & Hauser, 2001;
Hauser & Anderson, 1994; Petersen, Beecher, Zoloth, Moody, & Stebbins,
1978). Neurobiological studies confirmed some of these findings and, ad-
ditionally, identified the left Tpt area in macaques to be specifically in-
Figure 1. Schematic drawing of macaque (left), chimpanzee (mid) and human (right) brains
(left hemispheres) with Brodmann areas 44/45 and temporo-parietal areas (Tpt) indicated
(based on Amuts et al., 2010; Frey, Mackey, & Petrides, 2014; Gannon, Holloway, Broadfield,
&Braun, 1998; Schenker et al., 2008; Spocter et al., 2010). Images are not to scale.

Tracing the human brain's language areas
39
volved in the processing of conspecific calls (Hener & Hener, 1986;
Poremba et al., 2004). Rauschecker et al. (1995) demonstrated that pure
tones are processed at the core region of the superior temporal cortex
in macaques, whereas complex, species-specific vocalizations are pro-
cessed in more lateral regions.
A neuroimaging study measuring planum temporale activity of
chimpanzees during the perception of species-specific vocalizations
confirmed that the planum temporale region of the chimpanzee brain
is functionally specialized for the processing of species-specific vocal
signals, though no evidence was found for a lateralization eect (Tagli-
alatela, Russell, Schaeer, & Hopkins, 2009). The majority of studies on
nonhuman primates corroborate the fact that the temporal region of the
primate brain, including humans, is home to a voice recognition system
that is specialized in processing communication signals from conspecif-
ics (see, e.g., Belin, Zatorre, Lafaille, Ahad, & Pike, 2000; Petkov et al.,
2008; Spocter et al., 2010).
There is ample evidence indicating that species-specific communica-
tion signals of great apes are lateralized to the left cerebral hemisphere,
although the exact brain regions involved may be yet unclear. Studies
that directly measure neurological processes during communication
tasks are scarce (e.g., Taglialatela et al., 2009), but numerous behavioral
studies have revealed a trend of left-lateralization. Manual gestures in
most great apes seem to be governed by left-hemispheric structures (e.g.,
chimpanzees: Hobaiter & Byrne, 2013; Hopkins & Leavens, 1998; bonobos:
Hopkins & Vauclair, 2012) and the laterality eect may be even stron-
ger when vocalizations accompany these gestures (Hopkins & Cantero,
2003; Taglialatela, Russell, Schaeer, & Hopkins, 2011). Both Broca's and
Wernicke's areas have been implicated in those communicative process-
es. Hopkins and Nir (2011) and Spocter et al. (2010) identified a correla-
tion between the degree of asymmetry of the planum temporale and the
propensity for right-handedness of gestures in chimpanzees (Hopkins &
Nir, 2011; Spocter et al., 2010). Tagliatelata et al. (2006) described the
same correlation for gesture handedness and size of the inferior frontal
gyrus. As shown by Meguerditchian et al. (2012), both the planum tem-
porale and inferior frontal gyral surface asymmetry are correlated with
communicative gesture in chimpanzees. At the moment it is unclear
which of the two brain regions is more closely linked to communication.

Eva Maria Luef
40
Handedness, in general, has been described to be strongly associat-
ed with language in modern humans, with the majority of right-handed
people demonstrating left-hemispheric specialization for language func-
tion (Knecht et al., 2000). A study of hand preference in chimpanzees,
however, has shown that the neurobiological correlates of handedness in
chimpanzees do not seem to be related to the language areas (Hopkins &
Cantalupo, 2004). Handedness may have co-evolved with language only
during human evolution (Corballis, 2003), and the connection between
the two is possibly related to gestural communication or tool use (see,
e.g., Hopkins, Russell, & Cantalupo, 2007; Meguerditchian, Vauclair, &
Hopkins, 2013).
Broca's and Wernicke's areas and their nonhuman homologues are
not only dierent in size and situated in dierent cortical locations
across species, but are also characterized by dierences in their inter-
nal cell-makeup. Broca's area and the temporal plane in humans display
wider cortical minicolumns, and this is particularly pronounced in the
left hemisphere (Rilling & Stout, 2014). Moreover, notable dierenc-
es between the association networks of the language areas have been
described, with human Broca's areas displaying more extensive con-
nections to the temporal gyrus than the homologue in nonhuman pri-
mates' brains. Concerning white matter pathways, comparable frontal
connections can be found in humans and nonhuman primates, including
the superior longitudinal fasciculus, the uncinate fasciculus, the cingu-
lum, the arcuate fasciculus and the inferior fronto-occipital fasciculus
(de Schotten, Dell'Acqua, Valabregue, & Catani, 2012; Makris & Pandya,
2009; Rilling, Glasser, Jbabdi, Andersson, & Preuss, 2011). While some
of these pathways have been relatively preserved during the evolution of
great apes and humans, others were substantially reorganized. The tra-
jectory of the arcuate fasciculus, for instance, has been strongly modified
in human brains, linking the left frontal cortex to the middle and inferior
frontal gyri and parts of Broca's and Wernicke's areas (de Schotten et al.,
2012). In contrast, in macaques the terminal connection of the arcuate
fasciculus leads to areas of the visual cortex, whereas in chimpanzees
connections with the inferior parietal lobe (supramarginal and angular
gyri) are dominant (Rilling et al., 2008). This suggests that the cortical
organization and connections of the arcuate fasciculus have undergone
significant changes during human evolution by establishing connections

Tracing the human brain's language areas
41
to and from the core language areas, supposedly subserving linguistic
functions in the human brain.
In summary, the existing literature on the neurobiology of Broca's
and Wernicke's areas and their connections in human and nonhuman
primates notes a number of similarities as well as dierences between
the species. One of the key questions that now emerges is when the hu-
man-typical adaptations arose during human evolution.
4 PALEONEUROLOGY: LANGUAGE AREAS IN THE BRAINS OF
ARCHAIC HUMANS
As language is ubiquitous to all modern humans, it must at least date back
to before 200,000 years ago when all modern humans shared a common
ancestor (Cann, 2012). In line with evolutionary theory, language could
have been formed through gradual adaptations within the existing gene
pool of variation and without any extreme mutations prevailing to spread
to future generations (Bickerton, 2002).
Because of a lack of data, no definite evidence exists that could tell
us about the presumed communication systems of the extinct members
of the hominin group (i.e., the genus Homo) or the neurobiological cor-
relates of their linguistic ability. However, indirect evidence can be gath-
ered by studying brain morphology of archaic humans. This is possible
with skull imprints, so-called endocranial casts (or endocasts, see Figure
2) that show the indentations of the former brain and blood vessels on
the inside of the skull (Holloway, Broadfield, & Yuan, 2004). By using
this method, particular brain regions can be identified and analyzed in
terms of their size. Endocast studies are a standard methodology of pa-
leoneurology, but unfortunately, researchers are often confronted with
the problem of incomplete and fractured skulls from which sulcal in-
dentations can be dicult to determine. Therefore, a certain degree of
uncertainty is imminent to this method. Nonetheless, endocast models
are valuable and crucial tools for understanding hominin brain evolution
when very little direct evidence is available.
The immediate ancestors of humans, the Australopithecines, likely did
not appear until four million years ago during the Pliocene in East Africa

Eva Maria Luef
42
(see Figure 3; Leakey, Feibel, McDougall, Ward, & Walker, 1998). Their
cranial capacity was about 400–450 cubic centimeters (which is com-
parable to large chimpanzee brains) and tentative evidence suggests an
occipital asymmetry (Holloway, 1983). Concerning the language regions,
it is disputed whether Broca's area is clearly defined on Australopithe-
cine endocasts (Holloway, 1983). Falk (1980), for instance, sees enough
evidence for the argument that the Australopithecine Broca's area re-
sembles that of great apes. For Wernicke's area, only tentative evidence
exists. The assumed increase in the posterior parietal association cortex
of Australopithecine brains could have resulted in reorganization of cer-
tain temporal regions, including Wernicke's area, by around three mil-
lion years ago (Holloway, 1983; Spocter et al., 2010).
With the advent of the genus Homo, evidence for the core language
areas becomes clearer on endocasts. When exactly the first archaic hu-
man emerged has been a matter of discussion, though it is assumed that
by 1.9 million years ago Homo rudolfensis had appeared in East Africa
(Antón, Potts, & Aiello, 2014). Those bipedal, terrestrial creatures pos-
sessed a brain the size of around 530 cubic centimeters, and the endocast
of a famous skull from the Turkana Basin (KNM-ER 1470) shows clear
imprints of an asymmetric Broca's area similar to that of modern humans
(Holloway, 2015). Contemporary species to H. rudolfensis may have in-
Figure 2. Endocasts from Sambungmacan Homo erectus from Indonesia. Broca's area is en-
larged in the left hemisphere in comparison to the right one (reprinted from The Anatomical
Record, Vol. 262, Broadfield et al., Endocast of Sambungmacan 3, p. 375, Copyright (2001)
with permission from Wiley).

Tracing the human brain's language areas
43
cluded H. habilis and H. erectus/ergaster (Boyd & Silk, 2015), and endo-
casts of specimens of both species seem to demonstrate an asymmetric
enlargement in Broca's area (Harris, 1998; Tobias, 1998). Wernicke's area
is assumed to have resulted from the general growth of the superior tem-
poral areas (see, e.g., Oubre, 1997). H. erectus, the first human to expand
beyond Africa and a direct ancestor of modern humans (e.g., Sept, 2015),
had evolved larger brains (approximately 1,000 cubic centimeters) with
a clear left-occipital-right-frontal asymmetry and a pronounced Broca's
cap, as is characteristic for modern humans (Wu, Holloway, Schepartz, &
Xing, 2011). Wynn (1998) suggests that both Broca's and Wernicke's areas
in H. erectus were distinctly human-like.
Approximately 600,000 years ago, a new species appeared in Europe,
Homo heidelbergensis, which was only a bit smaller-brained (approxi-
mately 1,200 cubic centimeters) than modern humans (which is around
1,250 cubic centimeters, see, e.g., Boyd & Silk, 2015). Endocast prints
show that their brains were left-occipital-right-frontal asymmetric and
showed a prominent bulge in the left hemisphere over Broca's area (Hol-
loway et al., 2004). By 300,000 years ago, the evolutionary transition
began that would lead to Homo neanderthalensis in Europe. Neander-
thals had a brain larger than those of modern humans (approximately
1,500 cubic centimeters) and displayed a clear asymmetry in Broca's area
(Holloway, 2015; Jerison, 1997). According to Holloway (1985), Broca's
area is as developed on Neanderthal endocasts as it is in those of modern
humans. Homo sapiens altai (or Homo sapiens ssp. Denisova, or simply
Figure 3. Human family tree.

Eva Maria Luef
44
Denisovans), close relatives of Neanderthals and modern humans whose
fossils were recently discovered in Russia and China, had the largest
brains of all archaic humans known today (approximately 1,800 cubic
centimeters, Li et al., 2017). At present not much is known about Broca's
and Wernicke's areas in this species.
While left-hemispheric asymmetry is well established in archaic hu-
mans, its relation to language function is unclear. In an attempt to put
together more puzzle pieces to supplement the scarce data that exists on
the neurobiology of archaic humans' language capabilities, researchers
have started to include additional information from fossils that could be
relatable to linguistic function, such as hand preference (Steele & Uo-
mini, 2009). The archeological record can provide evidence for hand
preference of a species through material culture (tools, artefacts) as well
as through skeletal asymmetries resulting from preferential use of one
limb. Even though right-hand preference is suggested to date back as far
as 1.9 million years ago (Toth, 1985), the evidence becomes substantial
with H. heidelbergensis (Lozano, Mosquera, Bermudez de Castro, Arsua-
ga, & Carbonell, 2009) and the Neanderthals (Frayer et al., 2012; Uomini,
2011). Whether language and handedness evolved in tandem in archaic
hominins is dicult to answer based on the current data, and the exact
nature of the concatenation of language and handedness in hominins re-
mains unknown at present.
The existence of the modern core language areas in the brains of ar-
chaic humans is certainly tantalizing for research into language origins,
though the evidence is mostly uncertain or even highly speculative at
times. An enlarged Broca's cap, for instance, may also appear on endo-
casts of large chimpanzees, indicating that language does not need be
the driving force behind its increase (Holloway, 1983). More generally,
there is no evidence that these areas in archaic humans functioned as
speech/language centers. Without additional evidence regarding respi-
ratory control and vocal tract anatomy of a species, it is dicult to ascer-
tain solely from neuropaleontological data whether a species possessed
the abilities to develop a verbal form of proto-language (Deacon, 1997;
however see Fitch, De Boer, Mathur, & Ghazanfar, 2016). Anthropologi-
cal research often has to draw on circumstantial evidence to construct a
case for language in archaic hominins, connecting, for instance, the pro-
duction of art or tools to symbolic language.

Tracing the human brain's language areas
45
A new research avenue that has recently opened up is the inclusion
of genetics into the question of the origins of human language. Advances
in molecular technology have made it possible to start to relate specif-
ic brain regions to a set of underlying genes, whose expression directly
influences the development of that region. Relevant findings concern-
ing the neurobiology of language have resulted from this research and
the forkhead box protein p2 (known as FOXP2) has been suggested to
play a role in the functioning of Broca's and Wernicke's areas (Liégeois
et al., 2003). The gene has also been identified in Neanderthals (Krause
et al., 2007) and Denisovans (Meyer et al., 2012), which has spurred hy-
potheses on language abilities in those close relatives of modern humans.
Another recent gene discovery could make important contributions to
the genetics of language: GPR56 is strongly linked to the Sylvian fissure
language region, including Broca's area (Bae et al., 2014). New emerging
hypotheses on the genetics of language should take into account what
role the gene might have played during human evolution.
The field of language evolution has naturally suered from paucity of
data, due to the fact that cognitive abilities do not fossilize, and one way
forward can be seen in modern neurogenetics. Through the identification
of particular sets of genes that are crucial for the development of relevant
language areas in the human brain and by comparing those data to ge-
netic information gathered from extant nonhuman primates and extinct
hominins, new insights will be possible. The field of paleogenetics is only
just emerging as a key player in the evolution of language, but it may well
turn out to be the missing link between primatology, paleoanthropology
and modern linguistics that can move the field of language evolution for-
ward in the 21st century.
5 CONCLUSION
In modern humans, Broca's and Wernicke's areas are complex cerebral
regions mediating a versatile range of functions related to language. In
terms of their evolutionary history, it can be assumed that the new lin-
guistic functions of Homo sapiens brains arose most likely through the
modification of existing brain circuitry that was present in the last an-

Eva Maria Luef
46
cestor of humans. The neurobiological correlates of today's linguistic
abilities were built on pre-existing neural structures that subserved dif-
ferent cognitive abilities in primate history. It is the most likely evolu-
tionary scenario that Broca's and Wernicke's areas originally processed
information in ways that happened to be useful to language: Broca's area
may have evolved to extract and analyze sequential and motor patterns
while Wernicke's area may have evolved out of a more general ability to
analyze species-specific calls. Both of these skills make a useful substrate
for language to utilize and their neural connectivity and behavioral in-
terplay could have provided the crucial impetus for the development of
the linguistic mind.
 ACKNOWLEDGEMENTS
This work was made possible by the Research Resettlement Fund for New
Faculty and the Overhead Fund 2017 of the College of Education of Seoul
National University. I thank Jong-seung Sun for her help during the
preparation of the manuscript and the artist Jaehyeong Yoo who created
the drawings. In addition, I am grateful to five thoughtful reviewers who
provided valuable comments for improving the manuscript.
REFERENCES
Amuts, K., Lenzen, M., Friederici, A. D., Schleicher, A., Morosan, P., Palome-
ro-Gallagher, N., & Zilles, K. (2010). Broca's region: Novel organizational prin-
ciples and multiple receptor mapping. PLoS Biology, 8, e1000489.
Amuts, K., Schleicher, A., Burgel, U., Mohlberg, H., Uylings, H. B., & Zilles, K.
(1999). Broca's region revisited: Cytoarchitecture and intersubject variability.
Journal of Comparative Neurology, 412, 319–341.
Antón, S. C., Potts, R., & Aiello, L. C. (2014). Evolution of early Homo: An integrat-
ed biological perspective. Science, 345, 1–13.
Ardila, A., Bernal, B., & Rosselli, M. (2016). How localized are language brain ar-
eas? A review of Brodmann areas involvement in oral language. Archives of
Clinical Neuropsychology, 31, 112–122.

Tracing the human brain's language areas
47
Bae, B. I., Tietjen, I., Atabay, K. D., Evrony, G. D., Johnson, M. B., Asare, E., … Walsh,
C. A. (2014). Evolutionarily dynamic alternative splicing of GPR56 regulates
regional cerebral cortical patterning. Science, 343, 764–768.
Belin, P., Zatorre, R. J., Lafaille, P., Ahad, P., & Pike, B. (2000). Voice-selective areas
in human auditory cortex. Nature, 403, 309–312.
Ben Shalom, D., & Poeppel, D. (2008). Functional anatomic models of language:
Assembling the pieces. The Neuroscientist, 14, 119–127.
Benson, D. F., & Ardila, A. (1996). Aphasia. New York: Oxford University Press.
Bickerton, D. (2002). From protolanguage to language. In T. J. Crow (Ed.), The
speciation of modern homo sapiens (pp. 103–120). Oxford: Oxford University
Press.
Bidula, S. P., & Króliczak, G. (2015). Structural asymmetry of the insula is linked to
the lateralization of gesture and language. European Journal of Neuroscience,
41, 1438–1447.
Boyd, R., & Silk, J. B. (2015). How humans evolved. New York: W. W. Norton &
Company.
Broadfield, D. C., Holloway, R. L., Mowbray, K., Silvers, A., Yuan, M. S., & Mar-
quez, S. (2001). Endocast of Sambungmacan 3 (Sm3): A new Homo erectus
from Indonesia. The Anatomical Record: Advances in Integrative Anatomy and
Evolutionary Biology, 262, 369–379.
Broca, P. P. (1861). Remarques sur le siége de la faculté du langage articulé, suiv-
ies d'une observation d'aphemie (perte de la parole). Bulletin de la Société
Anatomique de Paris, 36, 330–357.
Broca, P. P. (1865). Sur le siège de la faculté du langage articulé. Bulletins de la So-
ciété d'anthropologie de Paris, 1, 377–393.
Burdach, K. (1822). Vom Bau und Leben des Gehirns und Rückenmarks. Leipzig: In
der Dyk‘schen Buchhandlung.
Cabanis, E. A., Iba-Zizen, M. T., Abelanet, R., Monod-Broca, P., & Signoret, J. L.
(1994). “Tan-Tan” the first Paul Broca's patient with “Aphemia” (1861): CT
(1979) and MRI (1994) of the brain. In L. Picard & G. Salamon (Eds.), 4th Re-
fresher Course of the ESNR: Language and Aphasias (pp. 9–22). Nancy: Europe-
an Society of Neuroradiology.
Cann, R. L. (2012). Molecular perspectives on human evolution. In K. R. Gibson &
M. Tallerman (Eds.), The Oxford handbook of language evolution (pp. 250–257).
Oxford: Oxford University Press.
Cantalupo, C., & Hopkins, W. D. (2001). Asymmetric Broca's area in great apes.
Nature, 414, 505.
Castaigne, P., Lhermitte, F., Signoret, J. L., & Abelanet, R. (1980). Description et
étude scanographique du cerveau du Leborgne: La découverte de Broca. Revue
Neurologique (Paris), 136, 563–583.
Catani, M., & Jones, D. K. (2005). Perisylvian language networks of the human
brain. Annals of Neurology, 57, 8–16.

Eva Maria Luef
48
Corballis, M. C. (2003). From mouth to hand: Gesture, speech, and the evolution
of right-handedness. Behavioral and Brain Sciences, 26, 208–260.
Cubelli, R., & Montagna, C. G. (1994). A reappraisal of the controversy of Dax and
Broca. Journal of the History of the Neurosciences, 3, 215–226.
de Bruin, A., Roelofs, A., Dijkstra, T., & Fitzpatrick, I. (2014). Domain-general in-
hibition areas of the brain are involved in language switching: FMRI evidence
from trilingual speakers. NeuroImage, 90, 348–359.
de Schotten, M. G., Dell'Acqua, F., Valabregue, R., & Catani, M. (2012). Monkey
to human comparative anatomy of the frontal lobe association tracts. Cortex,
48, 82–96.
Deacon, T. W. (1997). The symbolic species: The co-evolution of language and the
brain. New York: W. W. Norton & Company.
Dejerine, J. (1895). Anatomie des centres nerveux. Paris: Rue et Cie.
Dick, A. S., & Tremblay, P. (2012). Beyond the arcuate fasciculus: Consensus and
controversy in the connectional anatomy of language. Brain, 135, 3529–3550.
Dronkers, N. F., Plaisant, O., Iba-Zizen, M. T., & Cabanis, E. A. (2007). Paul Broca's
historical cases: High resolution MR imaging of the brains of Leborgne and
Lelong. Brain, 130, 1432–1441.
Dronkers, N. F., Redfern, B. B., & Ludy, C. A. (1995). Lesion localization in chronic
Wernicke's aphasia. Brain and Language, 51, 62–65.
Du, M. C., & Brown-Schmidt, S. (2017). Hippocampal contributions to language
use and processing. In D. E. Hannula & M. C. Du (Eds.), The hippocampus
from cells to systems: Structure, connectivity, and functional contributions to
memory and flexible cognition (pp. 503–536). Berlin: Springer.
Duau, H., Moritz-Gasser, S., & Mandonnet, E. (2014). A re-examination of neural
basis of language processing: Proposal of a dynamic hodotopical model from
data provided by brain stimulation mapping during picture naming. Brain and
Language, 131, 1–10.
Economo, C., & Koskinas, G. N. (1925). Die Cytoarchitektonik der Hirnrinde des
erwachsenen Menschen. Wien: Springer.
Embick, D., Marantz, A., Miyashita, Y., O'Neil, W., & Sakai, L. (2000). A syntactic
specialization for Broca's area. Proceeding of the National Academy of Sciences
USA, 97, 6150–6154.
Falk, D. (1980). A reanalysis of the South African australopithecine natural endo-
casts. American Journal of Physical Anthropology, 53, 525–539.
Falk, D. (2014). Interpreting sulci on hominin endocasts: Old hypotheses and new
findings. Frontiers in Human Neuroscience, 8, 134.
Fernández-Carriba, S., Loeches, A., Morcillo, A., & Hopkins, W. D. (2002). Asym-
metry in facial expression of emotions by chimpanzees. Neuropsychologia, 40,
1523–1533.
Finger, S. (2010). The birth of localization theory. In S. Finger, F. Boller, & K. L. Ty-
ler (Eds.), Handbook of clinical neurology (pp. 117–128). Amsterdam: Elsevier.

Tracing the human brain's language areas
49
Fitch, T. W., De Boer, B., Mathur, N., & Ghazanfar, A. A. (2016). Monkey vocal
tracts are speech-ready. Science Advances, 2, e1600723.
Frayer, D. W., Lozano, M., Bermudez de Castro, J. M., Carbonell, E., Arsuaga, J. L.,
Radovčić, J., … Bondioli, L. (2012). More than 500.000 years of right-handed-
ness in Europe. Laterality: Asymmetries of Body, Brain and Cognition, 17, 51–69.
Frey, S., Campbell, J. S., Pike, G. B., & Petrides, M. (2008). Dissociating the human
language pathways with high angular resolution diusion fiber tractography.
Journal of Neuroscience, 28, 11435–11444.
Frey, S., Mackey, S., & Petrides, M. (2014). Cortico-cortical connections of areas 44
and 45B in the macaque monkey. Brain and Language, 131, 36–55.
Friederici, A. D. (2002). Towards a neural basis of auditory sentence processing.
Trends in Cognitive Science, 6, 78–84.
Friederici, A. D. (2011). The brain basis of language processing: From structure to
function. Physiological Reviews, 91, 1357–1392.
Galaburda, A. M., & Pandya, D. N. (1982). Role of architectonics and connections in
the study of primate brain evolution. In D. Falk & E. Armstrong (Eds.), Primate
brain evolution: Methods and concepts (pp. 203–216). New York: Plenum Press.
Gallese, V. (2008). Mirror neurons and the social nature of language: The neural
exploitation hypothesis. Social Neuroscience, 3, 317–333.
Gannon, P. J., Holloway, R. L., Broadfield, D. C., & Braun, A. R. (1998). Asymmetry
of chimpanzee planum temporale: Humanlike pattern of Wernicke's brain lan-
guage area homolog. Science, 279, 220–222.
Gannon, P. J., Kheck, N., & Hof, P. R. (2008). Leftward interhemispheric asym-
metry of macaque monkey temporal lobe language area homolog is evident at
the cytoarchitectural, but not gross anatomic level. Brain Research, 1199, 62–73.
Geschwind, D. H., & Rakic, P. (2013). Cortical evolution: Judge the brain by its
cover. Neuron, 80, 633–647.
Geschwind, N. (1965). Disconnexion syndromes in animals and man. Brain, 88,
585–644.
Geschwind, N. (1970). The organization of language and the brain. Science, 170,
940–944.
Geschwind, N., & Levitsky, W. (1968). Human brain: Left-right asymmetries in
temporal speech region. Science, 161, 186–187.
Ghazanfar, A. A. (2008). Language evolution: Neural dierences that make a dif-
ference. Nature Neuroscience, 11, 382–384.
Ghazanfar, A. A., Smith-Rohrberg, D., & Hauser, M. D. (2001). The role of temporal
cues in rhesus monkey vocal recognition: Orienting asymmetries to reversed
calls. Brain, Behavior and Evolution, 58, 163–172.
Gibbs, R. A., Rogers, J., Katze, M. G., Bumgarner, R., Weinstock, G. M., Mardis, E.
R., … Zwieg, A. S. (2007). Evolutionary and biomedical insights from the rhe-
sus macaque genome. Science, 316, 222–234.

Eva Maria Luef
50
Gil-da-Costa, R., Martin, A., Lopes, M. A., Munoz, M., Fritz, J. B., & Braun, A. R.
(2006). Species-specific calls activate homologs of Broca's and Wernicke's
areas in the macaque. Nature Neuroscience, 9, 1064–1070.
Glasel, H., Leroy, F., Dubois, J., Hertz-Pannier, L., Mangin, J. F., & Dehaene-Lam-
bertz, G. (2011). A robust cerebral asymmetry in the infant brain: The right-
ward superior temporal sulcus. NeuroImage, 58, 716–723.
Graves, R. E. (1997). The legacy of the Wernicke-Lichtheim Model. Journal of the
History of the Neurosciences, 6, 3–20.
Guenther, F. H. (2016). Neural control of speech. Cambridge: MIT Press.
Harris, J. C. (1998). Developmental neuropsychiatry. New York: Oxford University
Press.
Hauser, M. D., & Anderson, K. (1994). Left hemisphere dominance for process-
ing vocalizations in adults, but not infant, rhesus monkeys: Field experiments.
Proceeding of the National Academy of Sciences USA, 91, 3946–3948.
Hauser, M. D., Chomsky, N., & Fitch, T. W. (2002). The faculty of language: What is
it, who has it, and how did it evolve? Science, 298, 1569–1579.
Hener, H. E., & Hener, R. S. (1986). Eect of unilateral and bilateral auditory
cortex lesions on the discrimination of vocalizations by Japanese macaques.
Journal of Neurophysiology, 56, 683–701.
Hickok, G. (2009). The functional neuroanatomy of language. Physics of Life Re-
views, 6, 121–143.
Hickok, G., & Poeppel, D. (2004). Dorsal and ventral streams: A framework for
understanding aspects of the functional anatomy of language. Cognition, 92,
67–99.
Hobaiter, C., & Byrne, R. W. (2013). Laterality in the gestural communication of
wild chimpanzees. Annals of the New York Academy of Sciences, 1288, 9–16.
Holloway, R. L. (1983). Human paleontological evidence relevant to language be-
havior. Human Neurobiology, 2, 105–114.
Holloway, R. L. (1985). The poor brain of Homo sapiens neanderthalensis: See
what you please. In E. Delson (Ed.), Ancestors: The hard evidence (pp. 319–
324). New York: A. R. Liss Inc.
Holloway, R. L. (2015). Brain evolution. In M. P. Muehlenbein (Ed.), Basics in hu-
man evolution (pp. 235–250). Amsterdam: Elsevier.
Holloway, R. L., Broadfield, D. G., & Yuan, M. S. (2004). The human fossil record.
Brain endocasts: The paleoneurological evidence. New Jersey: Wiley & Sons.
Hook-Costigan, M. A., & Roger, L. J. (1998). Lateralized use of the mouth in pro-
duction of vocalizations by marmosets. Neuropsychologia, 36, 1265–1273.
Hopkins, W. D., & Cantalupo, C. (2004). Handedness in chimpanyees (Pan trog-
lodytes) is associated with asymmetries of the primary motor cortex but not
with homologous language areas. Behavioral Neuroscience, 118, 1176–1183.

Tracing the human brain's language areas
51
Hopkins, W. D., & Cantero, M. (2003). From hand to mouth in the evolution of
language: The influence of vocal behavior on lateralized hand use in manual
gestures by chimpanzees (Pan troglodytes). Developmental Science, 6, 55–61.
Hopkins, W. D., Hopkins, A. M., Misiura, M., Latash, E. M., Mareno, M. C., Scha-
piro, S. J., & Phillips, K. A. (2016). Sex dierences in the relationship between
planum temporale asymmetry and corpus callosum morphology in chimpan-
zees (Pan troglodytes): A combined MRI and DTI analysis. Neuropsychologia,
93, 325–334.
Hopkins, W. D., & Leavens, D. A. (1998). Hand use and gestural communication in
chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 112, 95–99.
Hopkins, W. D., Marino, L., Rilling, J. K., & MacGregor, L. A. (1998). Planum tem-
porale asymmetries in great apes as revealed by magnetic resonance imaging
(MRI). NeuroReport, 9, 2913–2918.
Hopkins, W. D., & Nir, T. M. (2011). Planum temporale surface area and grey mat-
ter asymmetries in chimpanzees (Pan troglodytes): The eect of handedness
and comparison with findings in humans. Behavioural Brain Research, 208,
436–443.
Hopkins, W. D., Russell, J. L., & Cantalupo, C. (2007). Neuroanatomical correlates
of handedness for tool use in chimpanzees (Pan troglodytes). Psychological
Science, 18, 971–977.
Hopkins, W. D., & Vauclair, J. (2012). Evolution of behavioural and brain asymme-
tries in primates. In M. Tallerman & K. R. Gibson (Eds.), The Oxford handbook
of language evolution (pp. 184–197). Oxford: Oxford University Press.
Indefrey, P., & Levelt, W. J. M. (2004). The spatial and temporal signatures of word
production components. Cognition, 9, 101–144.
Jerison, H. J. (1997). Evolution of prefrontal cortex. In N. A. Krasnegor, R. Lyon,
& P. S. Goldman-Rakic (Eds.), Development of the prefrontal cortex: Evolution,
neurobiology, and behavior (pp. 9–26). Baltimore: Paul H. Brookes.
Keller, S. S., Roberts, N., Garcia-Finana, M., Mohammadi, S., Ringelstein, E.-B.,
Knecht, S., & Deppe, M. (2011). Can the language-dominant hemisphere be
predicted by brain anatomy? Journal of Cognitive Neuroscience, 23, 2013–2019.
Knecht, S., Dräger, B., Deppe, M., Bobe, L., Lohmann, H., Flöel, A., … Henningsen,
H. (2000). Handedness and hemispheric language dominance in healthy hu-
mans. Brain, 123, 2512–2518.
Kohler, E., Keysers, C., Umiltà, M. A., Fogassi, L., Gallese, V., & Rizzolatti, G.
(2002). Hearing sounds, understanding actions: Action representation in mir-
ror neurons. Science, 297, 846–848.
Krause, J., Lalueza-Fox, C., Orlando, L., Enard, W., Green, R. E., Burbano, H. A., …
Pääbo, S. (2007). The derived FOXP2 variant of modern humans was shared
with Neanderthals. Current Biology, 17, 1908–1912.
Langergraber, K., Prüfer, K., Rowney, C., Boesch, C., Crockford, C., Fawcett, K., …
Vigilant, L. (2012). Generation times in wild chimpanzees and gorillas suggest

Eva Maria Luef
52
earlier divergence times in great ape and human evolution. Proceeding of the
National Academy of Sciences USA, 109, 15716–15721.
Leakey, M. G., Feibel, C. S., McDougall, I., Ward, C., & Walker, A. (1998). New
specimens and confirmation of an early age for Australopithecus anamensis.
Nature, 393, 62–66.
Leroy, F., Cai, Q., Bogart, S. L., Dubois, J., Coulon, O., Monzalvo, K., … De-
haene-Lambertz, G. (2015). New human-specific brain landmark: The depth
asymmetry of superior temporal sulcus. Proceeding of the National Academy of
Sciences USA, 112, 1208–1213.
Li, Z.-Y., Wu, X.-J., Zhou, L.-P., Liu, W., Gao, X., Niam, X.-M., & Trinkaus, E. (2017).
Late pleistocene archaic human crania from Xuchang, China. Science, 355,
969–972.
Lichtheim, L. (1885). On aphasia. Brain, 7, 433–484.
Liégeois, F., Baldeweg, T., Connellly, A., Gadian, D. G., Mishkin, M., & Var-
gha-Khadem, F. (2003). Language fMRI abnormalities associated with FOXP2
gene mutation. Nature Neuroscience, 6, 1230–1237.
Locke, D. P., Hillier, L. W., Warren, W. C., Worley, K. C., Nazareth, L. V., Muzny, D.
M., … Wilson, R. K. (2011). Comparative and demographic analysis of orang-
utan genomes. Nature, 469, 529–533.
Losin, E. A. R., Russell, J. L., Freeman, H., Meguerditchian, A., & Hopkins, W. D.
(2008). Left hemisphere specialization for oro-facial movements of learned
vocal signals by captive chimpanzees. PLoS ONE, 3, e2529.
Lozano, M., Mosquera, M., Bermudez de Castro, J. M., Arsuaga, J. L., & Carbonell,
E. (2009). Right handedness of Homo heidelbergensis from Sima de los Hesos
Atapuerca, Spain 500,000 years ago. Evolution of Human Behavior, 30, 369–376.
Makris, N., & Pandya, D. N. (2009). The extreme capsule in humans and rethinking
of the language circuitry. Brain Structure and Function, 213, 343–358.
Marie, D., Roth, M., Lacoste, R., Nazarian, B., Bertello, A., Anton, J. L., … Meguer-
ditchian, A. (2017). Left brain asymmetry of the planum temporale in a non-
hominid primate: Redefining the origin of brain specialization for language.
Cerebral Cortex, 19, 1–8.
Meguerditchian, A., Gardner, M. J., Schapiro, S. J., & Hopkins, W. D. (2012). The
sound of one-hand clapping: Handedness and perisylvian neural correlates of
a communicative gesture in chimpanzees. Proceedings of the Royal Society B:
Biological Sciences, 279, 1959–1966.
Meguerditchian, A., Vauclair, J., & Hopkins, W. D. (2013). On the origins of hu-
man handedness and language: A comparative review of hand preferences for
bimanual coordinated actions and gestural communication in nonhuman pri-
mates. Developmental Psychobiology, 55, 637–650.
Meyer, M., Kircher, M., Gansauge, M. T., Li, H., Racimo, F., Mallick, S., … Pääbo, S.
(2012). A high-coverage genome sequence from an archaic Denisovan individ-
ual. Science, 338, 222–226.

Tracing the human brain's language areas
53
Meynert, T. (1867). Der Bau der Grosshirnrinde und seine örtlichen Verschieden-
heiten, nebst einem pathologisch-anatomischen Corollarium. Vierteljahres-
schrift fuer Psychiatrie, 1, 77–93.
Mohr, J. P., Pessin, M. S., Finkelstein, S., Funkenstein, H. H., Duncan, G. W., &
Davis, K. R. (1978). Broca aphasia: Pathological and clinical. Neurology, 28,
311–324.
Oubre, A. Y. (1997). Instinct and revelation: Reflections on the origins of numinous
perception. London: Taylor & Francis.
Papoutsi, M., de Zwart, J. A., Jansma, J. M., Pickering, J., Bednar, J. A., & Horwitz,
B. (2009). From phonemes to articulatory codes: An fMRI study of the role of
Broca's area in speech production. Cerebral Cortex, 19, 2156–2165.
Penfield, W., & Roberts, L. (1959). Speech and brain mechanisms. New Jersey:
Princeton University Press.
Petersen, M. R., Beecher, M. D., Zoloth, S. R., Moody, D. B., & Stebbins, W. C. (1978).
Neural lateralization of species-specific vocalizations by Japanese macaques
(Macaca fuscata). Science, 202, 324–327.
Petkov, C. I., Kayser, C., Steudel, T., Whittingstall, K., Augath, M., & Logothetis,
N. K. (2008). A voice region in the monkey brain. Nature Neuroscience, 11,
367–374.
Petrides, M. (2014). Neuroanatomy of language regions of the human brain. Am-
sterdam: Elsevier.
Petrides, M., Cadoret, G., & Mackey, S. (2005). Orofacial somatomotor responses
in the macaque monkey homnologue of Broca's area. Nature, 435, 1235–1238.
Petrides, M., & Pandya, D. N. (1988). Association fiber pathways to the frontal cor-
tex from the superior temporal region in the rhesus monkey. Journal of Com-
parative Neurology, 273, 52–66.
Poremba, A., Malloy, M., Saunders, R. C., Carson, R. E., Herscovitch, P., & Mishkin,
M. (2004). Species-specific calls evoke asymmetric activity in the monkey's
temporal poles. Nature, 427, 448–451.
Preuss, T. M. (2000). What's human about the human brain? In M. S. Gazzaniga
(Ed.), The new cognitive neurosciences (pp. 1219–1234). Cambridge: MIT Press.
Preuss, T. M., & Goldman-Rakic, P. S. (1991). Architectonics of the parietal and
temporal association cortex in the strepsirrhine primate Galago compared to
the anthropoid primate Macaca. Journal of Comparative Neurology, 310, 475–
506.
Price, C. J. (2000). Functional imaging studies of aphasia. In J. C. Mazziotta, A. W.
Toga, & R. S. J. Frackowiak (Eds.), Brain mapping: The disorders (pp. 181–200).
San Diego: Academic Press.
Price, C. J. (2012). A review and synthesis of the first 20 years of PET and fMRI
studies of heard speech, spoken language and reading. NeuroImage, 62, 816–
847.

Eva Maria Luef
54
Rauschecker, J. P. (2011). An expanded role for the dorsal auditory pathway in sen-
sorimotor control and integration. Hearing Research, 271, 16–25.
Rauschecker, J. P., & Tian, B. (2000). Mechanisms and streams for processing of
‘what’ and ‘where’ in auditory cortex. Proceeding of the National Academy of
Sciences USA, 97, 11800–11806.
Rauschecker, J. P., Tian, B., & Hauser, M. (1995). Processing of complex sounds in
the macaque nonprimary auditory cortex. Science, 268, 111–114.
Rilling, J. K. (2006). Human and nonhuman primate brains: Are they allometri-
cally scaled versions of the same design? Evolutionary Anthropology, 15, 65–77.
Rilling, J. K., Glasser, M. F., Jbabdi, S., Andersson, J., & Preuss, T. M. (2011). Con-
tinuity, divergence, and the evolution of brain language pathways. Frontiers in
Evolutionary Neuroscience, 3, 11.
Rilling, J. K., Glasser, M. F., Preuss, T. M., Ma, X., Zhao, T., Hu, X., & Behrens,
T. (2008). The evolution of the arcuate fasciculus revealed with comparative
DTI. Nature Neuroscience, 11, 382–384.
Rilling, J. K., & Stout, D. (2014). Evolution of the neural bases of higher cognitive
function in humans. In M. S. Gazzaniga & G. R. Mangun (Eds.), The cognitive
neurosciences (5th ed.). Cambridge: MIT Press.
Sarkissov, S. A., Filimono, I. N., Kononowa, E. P., Preobraschenskaja, I. S., &
Kukuew, L. A. (1955). Atlas of the cytoarchitectonics of the human cerebral cor-
tex. Moscow: Medgiz.
Saur, D., Kreher, B. W., Schnell, S., Kuemmerer, D., Kellmeyer, P., Vry, M. S., … Wei-
ller, C. (2008). Ventral and dorsal pathways for language. Proceedings of the
National Academy of Sciences USA, 105, 18035–18040.
Schenker, N. M., Buxhoeveden, D. P., Blackmon, W. L., Amuts, K., Zilles, K., & Se-
mendeferi, K. (2008). A comparative quantitative analysis of cytoarchitecture
and mimicolumnar organization in Broca's area in humans and great apes.
Journal of Comparative Neurology, 510, 117–128.
Schenker, N. M., Hopkins, W. D., Spocter, M. A., Garrison, A. R., Stimpson, C. D.,
Erwin, J. M., … Sherwood, C. C. (2010). Broca's area homologue in chimpan-
zees (Pan troglodytes): Probabilistic mapping, asymmetry, and comparison to
humans. Cerebral Cortex, 20, 730–742.
Schmahmann, J. D., Pandya, D. N., Wang, R. P., Dai, G., D'Arceuil, H., de Crespigny,
A. J., & Wedeen, V. J. (2007). Association fibre pathways of the brain: Paral-
lel observations from diusion spectrum imaging and autoradiography. Brain,
130, 630–653.
Schoenemann, P. T., Sheehan, M. J., & Glotzer, L. D. (2005). Prefrontal white mat-
ter volume is disproportionaly larger in humans than in other primates. Nature
Neuroscience, 8, 242–252.
Seiert, E. R., Perry, J. M. G., Simons, E. L., & Boyer, D. M. (2009). Convergent evo-
lution of anthropoid-like adaptations in Eocene adapiform primates. Nature,
461, 1118–1122.

Tracing the human brain's language areas
55
Semendeferi, K., Armstrong, E., Schleicher, A., Zilles, K., & Van Hoesen, G. W.
(1998). Limbic frontal cortex in hominoids: A comparative study of area 13.
American Journal of Physical Anthropology, 106, 129–155.
Semendeferi, K., Armstrong, E., Schleicher, A., Zilles, K., & Van Hoesen, G. W.
(2001). Prefrontal cortex in humans and apes: A comparative study of area 10.
American Journal of Physical Anthropology, 114, 224–241.
Sept, J. (2015). Early hominin ecology. In M. P. Muehlenbein (Ed.), Basics in hu-
man evolution (pp. 85–101). Amsterdam: Elsevier.
Sherwood, C. C., Broadfield, D. C., Holloway, R. L., Gannon, P. J., & Hof, P. R.
(2003). Variability of Broca's area homologue in African great apes: Implica-
tions for language evolution. The Anatomical Record: Advances in Integrative
Anatomy and Evolutionary Biology, 271, 276–285.
Sherwood, C. C., Subiaul, F., & Zawidzki, T. W. (2008). A natural history of the
human mind: Tracing evolutionary changes in brain and cognition. Journal of
Anatomy, 212, 426–454.
Silbert, L. J., Honey, C. J., Simony, E., Poeppel, D., & Hasson, U. (2014). Coupled
neural systems underlie the production and comprehension of naturalistic
narrative speech. Proceedings of the National Academy of Sciences USA, 111,
4687–4696.
Spocter, M. A., Hopkins, W. D., Garrison, A. R., Bauernfeind, A. L., Stimpson, C.
D., Hof, P. R., & Sherwood, C. C. (2010). Wernicke's area homologue in chim-
panzees (Pan troglodytes) and its relation to the appearance of modern human
language. Proceedings of the Royal Society B: Biological Sciences, 277, 2165–2174.
Steele, J., & Uomini, N. (2009). Can the archaeology of manual specialization tell
us anything about language evolution? A survey of the state of play. Cambridge
Archeological Journal, 19, 97–110.
Steinmetz, H., & Seitz, R. J. (1991). Functional anatomy of language processing:
Neuroimaging and the problem of individual variability. Neuropsychologia, 29,
1149–1161.
Taglialatela, J. P., Cantalupo, C., & Hopkins, W. D. (2006). Gesture handedness
predicts asymmetry in the chimpanzee inferior frontal gyrus. NeuroReport, 17,
923–927.
Taglialatela, J. P., Russell, J., Schaeer, J., & Hopkins, W. D. (2008). Communica-
tive signaling activates “Broca's” homolog in chimpanzees. Current Biology, 18,
343–348.
Taglialatela, J. P., Russell, J. L., Schaeer, J. A., & Hopkins, W. D. (2009). Visual-
izing vocal perception in the chimpanzee brain. Cerebral Cortex, 19, 1151–1157.
Taglialatela, J. P., Russell, J. L., Schaeer, J. A., & Hopkins, W. D. (2011). Chimpan-
zee vocal signaling points to a multimodal origin of human language. PLoS
ONE, 6, e18852.

Eva Maria Luef
56
Talairach, J., & Tournoux, P. (1988). Co-planar stereotactic atlas of the human
brain: 3-dimensional proportional system – An approach to cerebral imaging.
New York: Thieme Medical Publishers.
Tiedt, H. O., Ehlen, F., Krugel, L. K., Horn, A., Kuehn, A. A., & Klostermann, F.
(2017). Subcortical roles in lexical task processing: Inferences from thalamic
and subthalamic event-related potentials. Human Brain Mapping, 38, 370–383.
Tobias, P. (1998). Evidence for the early beginnings of spoken language. Cambridge
Archeological Journal, 8, 72–78.
Toga, A. W., & Thompson, P. M. (2003). Mapping brain asymmetry. Nature Re-
views Neuroscience, 4, 37–48.
Toth, N. (1985). Archaeological evidence for preferential right-handedness in the
lower and middle pleistocene, and its possible implications. Journal of Human
Evolution, 14, 607–614.
Ungerleider, L. G., & Haxby, J. V. (1994). ‘What’ and ‘where’ in the human brain.
Current Opinion in Neurobiology, 4, 157–165.
Uomini, N. T. (2011). Handedness in Neanderthals. In N. J. Conard & J. Richter
(Eds.), Neanderthal lifeways, subsistence and technology (pp. 139–154). Heidel-
berg: Springer.
Vauclair, J. (2004). Lateralization of communicative signals in nonhuman pri-
mates and the hypothesis of the gestural origin of language. Interaction
Studies, 5, 363–384.
Weiller, C., Bormann, T., Saur, D., Musso, M., & Rijntjes, M. (2011). How the ventral
pathway got lost – and what its recovery might mean. Brain and Language, 118,
29–29.
Wernicke, C. (1874). Der aphasische Symptomencomplex: Eine psychologische
Studie auf anatomischer Basis. Breslau: M. Cohn & Weigert.
Wernicke, C. (1881). Lehrbuch der Gehirnkrankheiten: Für Ärzte und Studierende.
Kassel: Theodor Fischer.
Wilson, B., & Petkov, C. I. (2011). Communication and the primate brain: Insights
from neuroimaging studies in humans, chimpanzees and macaques. Human
Biology, 83, 175–189.
Wu, X., Holloway, R. L., Schepartz, L. A., & Xing, S. (2011). A new brain endocast of
Homo erectus from Hulu Cave, Nanjing, China. American Journal of Physical
Anthropology, 145, 452–460.
Wynn, T. (1998). Did Homo erectus speak? Cambridge Archeological Journal, 8,
78–81.