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A) Diagram showing the path of the pyramidal cell (black) apical dendrite with respect to the anterior (1), lateral (2), and basal (3) aspect of the accessory olfactory bulb (shaded, egg-shaped). (B) Dendritic trajectory of a pyramidal-like cell with respect to the accessory olfactory bulb (lighter) in a coronal view (lateral, right side). (C) Dorsal view.
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This study describes the microscopic organization of a wedge-shaped area at the intersection of the main (MOB) and accessory olfactory bulbs (AOBs), or olfactory limbus (OL), and an additional component of the anterior olfactory nucleus or alpha AON that lies underneath of the AOB. The OL consists of a modified bulbar cortex bounded anteriorly by t...
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... The link between the fox OL with the VNS and the strategic location of the OL between the AOB and the MOB suggest that the fox OL may be involved in the processing of specific stimuli signaling relevant intraspecific socio-sexual cues, similar to the suggested functionality of this region in laboratory rodents (Weruaga et al., 2001;Leinders-Zufall et al., 2007;Larriva-Sahd, 2012;Vargas-Barroso et al., 2017). ...
Introduction: The olfactory system in most mammals is divided into several subsystems based on the anatomical locations of the neuroreceptor cells involved and the receptor families that are expressed. In addition to the main olfactory system and the vomeronasal system, a range of olfactory subsystems converge onto the transition zone located between the main olfactory bulb (MOB) and the accessory olfactory bulb (AOB), which has been termed the olfactory limbus (OL). The OL contains specialized glomeruli that receive noncanonical sensory afferences and which interact with the MOB and AOB. Little is known regarding the olfactory subsystems of mammals other than laboratory rodents.
Methods: We have focused on characterizing the OL in the red fox by performing general and specific histological stainings on serial sections, using both single and double immunohistochemical and lectin-histochemical labeling techniques.
Results: As a result, we have been able to determine that the OL of the red fox ( Vulpes vulpes ) displays an uncommonly high degree of development and complexity.
Discussion: This makes this species a novel mammalian model, the study of which could improve our understanding of the noncanonical pathways involved in the processing of chemosensory cues.
... All these olfactory subsystems converge to the transition zone located between the main olfactory bulb and the accessory olfactory bulb. This area consists of a modified bulbar cortex bounded anteriorly by the dorsal MOB and posteriorly by the anterior AOB (Larriva-Sahd 2012). This area has been termed olfactory limbus (OL), and includes specialized glomeruli which receive uncanonical sensory afferences and interact with the MOB and AOB, opening the possibility that OL is a site of non-olfactory and atypical vomeronasal sensory integration (Vargas-Barroso et al., 2017). ...
... The connection of the fox olfactory limbus with the vomeronasal system and its strategic position between the main and accessory olfactory bulbs suggests that the fox's OL is involved in the processing of specific stimuli that signal relevant intraspecifical socio-sexual cues in line with what has been suggested by other authors in laboratory rodents (Weruaga et al., 2001;Leinders-Zufall et al., 2007;Larriva-Sahd, 2012;Vargas-Barroso et al., 2017). ...
The mammalian olfactory systems can be divided into several subsystems based on the anatomical location of their neuroreceptor cells and the family of receptors they express. The more in depth studied systems are the main olfactory system and the vomeronasal system, whose first integrative enters are the main and the accessory olfactory bulb, respectively. In addition, there is a range of olfactory subsystems which converge to the transition zone located between the main olfactory bulb and the accessory olfactory bulb., which has been termed as olfactory limbus (OL) and includes specialized glomeruli which receive uncanonical sensory afferences and interact with the MOB and AOB. Beyond the laboratory rodents, there is a lack of information regarding the olfactory subsystems of carnivores. We have focused on the specific study of the olfactory limbus of the fox, performing serial histological sections, general and specific histological stainings, including both double and simple immunohistochemical and lectin-histochemical labeling techniques. As a result, we have been able to determine that the OL of the fox shows an uncommon development with a high degree of development and complexity. This makes this species a novel mammalian model that could provide a wider understanding of non-canonical pathways involved in the processing of chemosensory cues.
... The anti-CR pattern of immunolabelling in the MOB glomeruli ( Figure 11) revealed the striking and intense immunolabelling of PG cells; however, in the neuropil, the anti-CR staining intensity was very weak, except for isolated subpopulations of unrelated glomeruli located in the vicinity of the AOB, which showed strong anti-CR immunostaining. Based on their location, these atypical glomeruli might be involved in the processing of chemical signals from the VNN, as has been hypothesized for the mouse olfactory limb glomeruli [129]. The presence of atypical glomeruli in the MOB is not a novel finding, as some examples have been described in the past, such as the necklace complex in mice [130] or the subset of glomeruli with high acetylcholinesterase reactivity [131]. ...
We approached the study of the main (MOB) and accessory olfactory bulbs (AOB) of the meerkat (Suricata suricatta) aiming to fill important gaps in knowledge regarding the neuroanatomical basis of olfactory and pheromonal signal processing in this iconic species. Microdissection techniques were used to extract the olfactory bulbs. The samples were subjected to hematoxylin-eosin and Nissl stains, histochemical (Ulex europaeus agglutinin, Lycopersicon esculentum agglutinin) and immunohistochemical labelling (Gαo, Gαi2, calretinin, calbindin, olfactory marker protein, glial fibrillary acidic protein, microtubule-associated protein 2, SMI-32, growth-associated protein 43). Microscopically, the meerkat AOB lamination pattern is more defined than the dog’s, approaching that described in cats, with well-defined glomeruli and a wide mitral-plexiform layer, with scattered main cells and granular cells organized in clusters. The degree of lamination and development of the meerkat MOB suggests a macrosmatic mammalian species. Calcium-binding proteins allow for the discrimination of atypical glomerular subpopulations in the olfactory limbus between the MOB and AOB. Our observations support AOB functionality in the meerkat, indicating chemosensory specialization for the detection of pheromones, as identified by the characterization of the V1R vomeronasal receptor family and the apparent deterioration of the V2R receptor family.
... Following the Valverde criteria, we have named them the γ and δ groups. The anterior positioning of these additional groups makes it very unlikely that they are associated with the AON, supporting the observations of Larriva-Sahd (2012), who associated the α group with the second-order processing of olfactory and vomeronasal information. Future studies should address the roles played by these unique neuronal formations. ...
The accessory olfactory bulb (AOB) is the first neural integrative centre of the vomeronasal system (VNS), which is associated primarily with the detection of semiochemicals. Although the rabbit is used as a model for the study of chemocommunication, these studies are hampered by the lack of knowledge regarding the topography, lamination, and neurochemical properties of the rabbit AOB. To fill this gap, we have employed histological stainings: lectin labelling with Ulex europaeus (UEA-I), Bandeiraea simplicifolia (BSI-B4), and Lycopersicon esculentum (LEA) agglutinins, and a range of immunohistochemical markers. Anti-G proteins Gαi2/Gαo, not previously studied in the rabbit AOB, are expressed following an antero-posterior zonal pattern. This places Lagomorpha among the small groups of mammals that conserve a double-path vomeronasal reception. Antibodies against olfactory marker protein (OMP), growth-associated protein-43 (GAP-43), glutaminase (GLS), microtubule-associated protein-2 (MAP-2), glial fibrillary-acidic protein (GFAP), calbindin (CB), and calretinin (CR) characterise the strata and the principal components of the BOA, demonstrating several singular features of the rabbit AOB. This diversity is accentuated by the presence of a unique organisation: four neuronal clusters in the accessory bulbar white matter, two of them not previously characterised in any species (the γ and δ groups). Our morphometric study of the AOB has found significant differences between sexes in the numerical density of principal cells, with larger values in females, a pattern completely opposite to that found in rats. In summary, the rabbit possesses a highly developed AOB, with many specific features that highlight the significant role played by chemocommunication among this species.
... Overall, the discovery of gene families encoding receptors that bind specific non-canonical stimuli adds up to the already complex organization of the MOS and AOS (Fülle et al., 1995;Liberles and Buck, 2006;Leinders-Zufall et al., 2007;Johnson et al., 2012;Larriva-Sahd, 2012;Thompson et al., 2012;Greer et al., 2016). Incidentally, the view that flight or fight behaviors are mediated by the MOB was unsuspected some decades ago (Raisman, 1971;Baxi et al., 2006). ...
... Overlapping responses and converging pathways within the olfactory bulbs (Vargas-Barroso et al., 2016) offer alternative substrates to understand influences of uncanonical sensory cues (see above) upon the MOS and AOS (Larriva-Sahd, 2012;Nicol et al., 2014;Matsuo et al., 2015;Greer et al., 2016), as commented next. ...
... As discussed earlier, the OL receives afferent information from a variety of sensory organs and neurons expressing all known OR families (see above; Fülle et al., 1995;Liberles and Buck, 2006;Leinders-Zufall et al., 2007;Johnson et al., 2012;Larriva-Sahd, 2012;Thompson et al., 2012;Greer et al., 2016). First, neurons expressing TAARs have been reported in the OE and the GG and shown to project to the postero-dorsal region of the MOB that includes the NGs (Storan and Key, 2006;Johnson et al., 2012;Pacifico et al., 2012). ...
The rodent main and accessory olfactory systems (AOS) are considered functionally and anatomically segregated information-processing pathways. Each system is devoted to the detection of volatile odorants and pheromones, respectively. However, a growing number of evidences supports a cooperative interaction between them. For instance, at least four non-canonical receptor families (i.e., different from olfactory and vomeronasal receptor families) have been recently discovered. These atypical receptor families are expressed in the sensory organs of the nasal cavity and furnish parallel processing-pathways that detect specific stimuli and mediate specific behaviors as well. Aside from the receptor and functional diversity of these sensory modalities, they converge into a poorly understood bulbar area at the intersection of the main- main olfactory bulb (MOB) and accessory olfactory bulb (AOB) that has been termed olfactory limbus (OL). Given the intimate association the OL with specialized glomeruli (i.e., necklace and modified glomeruli) receiving uncanonical sensory afferences and its interactions with the MOB and AOB, the possibility that OL is a site of non-olfactory and atypical vomeronasal sensory decoding is discussed.
... An important example of this is the interaction between the main-(MOS) and accessory olfactory (AOS) systems (Suárez et al., 2012;Baum and Larriva-Sahd, 2014). In fact, volatile and pheromonal stimuli that are sensed by the MOS and AOS, respectively, bring about functionally and behaviorally overlapping responses in these systems (Sam et al., 2001;Trinh and Storm, 2003;Lin et al., 2004;Xu et al., 2005;Spehr et al., 2006;Larriva-Sahd, 2008, 2012b. In the absence of a structural interaction between the main olfactory epithelium (MOE) and the vomeronasal organ (VNO) or between the main-(MOB) and accessory olfactory (AOB) bulbs, synergistic responses of the MOS and AOB are largely attributed to the anatomical overlap beyond these primary and secondary sensory structures, respectively (Boehm et al., 2005;Kang et al., 2011). ...
It is accepted that the main- and accessory- olfactory systems exhibit overlapping responses to pheromones and odorants. We performed whole-cell patch-clamp recordings in adult rat olfactory bulb slices to define a possible interaction between the first central relay of these systems: the accessory olfactory bulb (AOB) and the main olfactory bulb (MOB). This was tested by applying electrical field stimulation in the dorsal part of the MOB while recording large principal cells (LPCs) of the anterior AOB (aAOB). Additional recordings of LPCs were performed at either side of the plane of intersection between the aAOB and posterior-AOB (pAOB) halves, or linea alba, while applying field stimulation to the opposite half. A total of 92 recorded neurons were filled during whole-cell recordings with biocytin and studied at the light microscope. Neurons located in the aAOB (n = 6, 8%) send axon collaterals to the MOB since they were antidromically activated in the presence of glutamate receptor antagonists (APV and CNQX). Recorded LPCs evoked orthodromic excitatory post-synaptic responses (n = 6, aAOB; n = 1, pAOB) or antidromic action potentials (n = 8, aAOB; n = 7, pAOB) when applying field stimulation to the opposite half of the recording site (e.g., recording in aAOB; stimulating in pAOB, and vice-versa). Observation of the filled neurons revealed that indeed, LPCs send axon branches that cross the linea alba to resolve in the internal cellular layer. Additionally, LPCs of the aAOB send axon collaterals to dorsal-MOB territory. Notably, while performing AOB recordings we found a sub-population of neurons (24% of the total) that exhibited voltage-dependent bursts of action potentials. Our findings support the existence of: 1. a direct projection from aAOB LPCs to dorsal-MOB, 2. physiologically active synapses linking aAOB and pAOB, and 3. pacemaker-like neurons in both AOB halves. This work was presented in the form of an Abstract on SfN 2014 (719.14/EE17).
... Histological evaluation of the injection sites [64][65][66], as well as thiazine red staining [67][68][69] were performed as follows: Animals were anesthetized with sodium pentobarbital (50 mg/kg i.p.), transcardially perfused with 250 ml of 0.9% NaCl followed by 250 ml of 4% paraformaldehyde in 0.1 M phosphate buffer (pH 7.4), and brains were removed and prepared for the histological procedure, as described previously [64,65]. Sagittal sections (50 µm thick) were stained either with toluidine-blue [66] to verify the injection sites or with thiazine red to look for Aβ deposits [67][68][69]. ...
... Histological evaluation of the injection sites [64][65][66], as well as thiazine red staining [67][68][69] were performed as follows: Animals were anesthetized with sodium pentobarbital (50 mg/kg i.p.), transcardially perfused with 250 ml of 0.9% NaCl followed by 250 ml of 4% paraformaldehyde in 0.1 M phosphate buffer (pH 7.4), and brains were removed and prepared for the histological procedure, as described previously [64,65]. Sagittal sections (50 µm thick) were stained either with toluidine-blue [66] to verify the injection sites or with thiazine red to look for Aβ deposits [67][68][69]. ...
Early olfactory dysfunction has been consistently reported in both Alzheimer's disease (AD) and in transgenic mice that reproduce some features of this disease. In AD transgenic mice, alteration in olfaction has been associated with increased levels of soluble amyloid beta protein (Aβ) as well as with alterations in the oscillatory network activity recorded in the olfactory bulb (OB) and in the piriform cortex. However, since AD is a multifactorial disease and transgenic mice suffer a variety of adaptive changes, it is still unknown if soluble Aβ, by itself, is responsible for OB dysfunction both at electrophysiological and behavioral levels. Thus, here we tested whether or not Aβ directly affects OB network activity in vitro in slices obtained from mice and rats and if it affects olfactory ability in these rodents. Our results show that Aβ decreases, in a concentration- and time-dependent manner, the network activity of OB slices at clinically relevant concentrations (low nM) and in a reversible manner. Moreover, we found that intrabulbar injection of Aβ decreases the olfactory ability of rodents two weeks after application, an effect that is not related to alterations in motor performance or motivation to seek food and that correlates with the presence of Aβ deposits. Our results indicate that Aβ disrupts, at clinically relevant concentrations, the network activity of the OB in vitro and can trigger a disruption in olfaction. These findings open the possibility of exploring the cellular mechanisms involved in early pathological AD as an approach to reduce or halt its progress.
... To accomplish this, brain specimens of adult rat that had previously been submitted to electrolytic lesion of the olfactory bulb, were incubated with primary antibodies to the enzyme glutamate decarboxylase isoform 67 (GAD 67) and the immunoreactive sites (GAD67-I) visualized with the pre-embedding immunocytocehmical technique. Complementary, a large set of adult rodent brain specimens from our archive (Larriva-Sahd, 2004, 2006, 2008, 2010, 2012Marcellino et al., 2012) was freely utilized to define the general organization of the PC. 6. Survey micrograph from the neuropil in sublayer Ia of the piriform cortex. Numerous medium-caliber dendrites (Sh), axo-shaft (arrows), and axo-spinous (circles) are shown. ...
... Twenty-eight satisfactorily impregnated specimens from our archive of adult rat brain specimens (Larriva-Sahd, 2004, 2006, 2008, 2010, 2012 were analyzed in this part of the study. All experimental subjects consisted of 10-week old Wistar rats from either sex. ...
... For time to time, the usefulness of the Golgi technique is denied (Eyre, et al., 2008); however, for the last ten years a number of novel neurons and neural organizing principles have been offered by this ancient technique, even in the adult rodent (Larriva-Sahd, 2004, 2006, 2008, 2012Paredes and Larriva-Sahd, 2010;Marcellino, et al., 2012) and human nervous system (Dall'oglio, et al., 2013). The PC should not be excluded (Larriva-Sahd, 2010). ...
The microscopic organization of the piriform cortex (PC) was studied in normal and experimental material from adult albino rats. In rapid-Golgi specimens a set of collaterals from the lateral olfactory tract (i.e., sublayer Ia) to the neuropil of the Layer II (LII) was identified. Specimens from experimental animals that received electrolytic lesion of the main olfactory bulb three days before sacrificing, were further processed for pre-embedding immunocytochemistry to the enzyme glutamic acid decarboxylase 67 (GAD 67). This novel approach permitted a simultaneous visualization at electron microscopy of both synaptic degeneration and GAD67-immunoreactive (GAD-I) sites. Degenerating and GAD-I synapses were separately found in the neuropil of Layers I and II of the PC. Previously overlooked patches of neuropil were featured in sublayer Ia. These areas consisted of dendritic and axonal processes including four synaptic types. Tridimensional reconstructions from serial thin sections from LI revealed the external appearance of the varicose and tubular dendrites as well as the synaptic terminals therein. The putative source(s) of processes to the neuropil of sublayer Ia is discussed in the context of the internal circuitry of the PC and an alternative model is introduced Anat Rec, 2013. © 2013 Wiley Periodicals, Inc.
... Importantly, through projections via the anterior limb of the anterior commissure (ALAC), the AON also can regulate the contralateral AON, OB, and APC. The two other structures, the ventral tenia tecta and dorsal peducular cortex, extend into the region dorsal to the peduncle, and have received little attention (Haberly, 2001;Brunjes et al., 2005;Larriva-Sahd, 2012). ...
The central core of the olfactory peduncle [the tissue connecting the olfactory bulb (OB) to the forebrain] includes a white matter tract that extends caudally to the anterior commissure (AC). The purpose of the present study was to examine this "anterior limb of the anterior commissure" (ALAC) to determine if the axons that progress through it segregate on the basis of their point of origin, neurotransmitter type, size, or shape. While local differences in axon density were observed in the ALAC, they were not consistent between samples of the anterior and posterior peduncle, and no other compartmentalization within the tract was observed. The innervation of the caudal olfactory peduncle by neuromodulatory fibers was examined to determine if they enter the region via the ALAC. Cholinergic fibers (CHAT) densely filled the peduncle, followed in order by serotonergic, noradrenergic, histaminergic, and orexinergic processes. Differences in the distribution of the fibers were noted for each system. While each axon type could be observed in the ALAC, it is probable that they enter the peduncle though several routes. Data for axon caliber in the ALAC was compared to information previously collected on the peduncle's other white matter region, the lateral olfactory tract (LOT). Axons in the ALAC were smaller, suggesting that the olfactory system is organized with a fast system for distributing incoming sensory information and a more economical, distributed system for subsequent processing.
Cytological characteristics of a cell sharing structure of both an astrocyte and a neuron, here termed amphomorphic cell (AC), were defined here in adult rat rostral migratory stream (RMS). The AC perikayon corresponds to that of the B1 cell of the adult mouse subventricular zone (SVZ)-RMS. The AC and its processes are confined to the RMS. Each AC originates four sets of processes that overlap with those from its homologues and adjacent neural and stromal elements. ACs interact between them via reciprocal sets of processes: those directed caudally bear spheroidal vesicles (SVP) and form gap junctions with pleomorphic vesicles (PVs) associated with the anterior set from the adjacent AC. Large asymmetric synapses, a set of them arising from the anterior olfactory nucleus, converge on each SV. The interlacing processes of the AC, together with a set of perikaryal out-growths form the glial cuff surrounding migrating neuroblasts described earlier. Small asymmetrical and symmetrical synapses terminate in subsets of differentiated A-cells, termed here A1, in the bulbar part of the RMS. Both AC- and A1-cells form electrical synapses between them and with their homologues. The strategic, wide-spread distribution between the neuropil and blood vessels of the AC, its processes, and migrating neuroblasts, suggests that the AC might mediate between both endogenous inductors and neurotransmitters, influencing the adult-born neurons it had previously originated.
