Segregated pathways to the vomeronasal amygdala: differential projections from the anterior and posterior divisions of the accessory olfactory bulb

Apically and basally located receptor neurons in the vomeronasal sensory epithelium express G(i2 alpha)- and G(o alpha)-proteins, V1R and V2R vomeronasal receptors, project to the anterior and posterior accessory olfactory bulb and respond to different stimuli, respectively. The extent to which secondary projections from the two portions of the accessory olfactory bulb are convergent in the vomeronasal amygdala is controversial. This issue is addressed by using anterograde and retrograde tract-tracing methods in rats including electron microscopy. Injections of dextran-amines, Fluoro Gold, cholera toxin-B subunit and Fast Blue were delivered to the anterior and posterior accessory olfactory bulb, bed nucleus of the stria terminalis, dorsal anterior amygdala and bed nucleus of the accessory olfactory tract/anteroventral medial amygdaloid nucleus. We have demonstrated that, apart from common vomeronasal-recipient areas, only the anterior accessory olfactory bulb projects to the bed nucleus of the stria terminalis, medial division, posteromedial part, and only the posterior accessory olfactory bulb projects to the dorsal anterior amygdala and deep cell layers of the bed nucleus of the accessory olfactory tract and the anteroventral medial amygdaloid nucleus. These results provide evidence that, excluding areas of convergence, the V1R and V2R vomeronasal pathways project to specific areas of the amygdala. These two vomeronasal subsystems are therefore anatomically and functionally separated in the telencephalon.     

Afferent and efferent projections of the anterior cortical amygdaloid nucleus in the mouse

The anterior cortical amygdaloid nucleus (ACo) is a chemosensory area of the cortical amygdala that receives afferent projections from both the main and accessory olfactory bulbs. The role of this structure is unknown, partially due to a lack of knowledge of its connectivity. In this work, we describe the pattern of afferent and efferent projections of the ACo by using fluorogold and biotinylated dextranamines as retrograde and anterograde tracers, respectively. The results show that the ACo is reciprocally connected with the olfactory system and basal forebrain, as well as with the chemosensory and basomedial amygdala. In addition, it receives dense projections from the midline and posterior intralaminar thalamus, and moderate projections from the posterior bed nucleus of the stria terminalis, mesocortical structures and the hippocampal formation. Remarkably, the ACo projects moderately to the central nuclei of the amygdala and anterior bed nucleus of the stria terminalis, and densely to the lateral hypothalamus. Finally, minor connections are present with some midbrain and brainstem structures. The afferent projections of the ACo indicate that this nucleus might play a role in emotional learning involving chemosensory stimuli, such as olfactory fear conditioning. The efferent projections confirm this view and, given its direct output to the medial part of the central amygdala and the hypothalamic ‘aggression area’, suggest that the ACo can initiate defensive and aggressive responses elicited by olfactory or, to a lesser extent, vomeronasal stimuli.     

Lateral and medial amygdala of anuran amphibians and their relation to olfactory and vomeronasal information

The amygdala of anurans is currently considered as a complex of nuclei that share many features with their counterparts in amniotes. In the present study, the subdivisions of the amygdala that are directly related to olfactory and vomeronasal information, were investigated in the anurans Rana perezi and Xenopus laevis. In particular, the connectivity of the main and accessory olfactory bulbs and their related amygdaloid nuclei was studied by means of in vivo and in vitro tract-tracing with dextran amines. The projections observed from the main olfactory bulb clearly innervate the newly redefined lateral amygdala within the ventral pallium and, to a lesser extent, the rostral portion of the medial amygdala. Injections into the accessory olfactory bulb exclusively revealed projections to the medial amygdala. Tracer applications into the lateral and medial nuclei revealed abundant intra-amygdaloid connections. The dual flow of olfactory and vomeronasal projections throughout the telencephalon was not strictly segregated since the lateral pallium and the lateral amygdala, both receiving olfactory information, were found to project to the medial amygdala (the only target of vomeronasal information), which in turn projects to the lateral amygdala. Additionally, both the lateral and the medial amygdala strongly project to the hypothalamus through the anuran equivalent of the stria terminalis. The main hodological features found in the present study suggest that forerunners of the olfactory and vomeronasal amygdaloid nuclei can be distinguished in anurans. This supports the notion that all tetrapods share a common pattern of organization of the amygdaloid complex, which links environmental (olfactory/vomeronasal) information and the behavioural response of the animal.     

Vomeronasal and olfactory pathways to the amygdala controlling male hamster sexual behavior: Autoradiographic and behavioral analyses

Previous studies suggest that the rostral corticomedial amygdala (CMA), particularly the medial nucleus, is an important site where vomeronasal and olfactory stimuli critical to male hamster copulatory behavior are processed. To test the possibility that mating deficits seen after lesions of the rostrally-placed medial nucleus may be due to the interruption of chemosensory afferents to more caudal areas, we injected tritiated amino acids into the accessory and main olfactory bulbs of male hamsters in which we had first produced bilateral electrolytic lesions or sham lesions in either the rostral CMA or basolateral amygdala, and then observed mating behavior. Autoradiographic analysis of ‘vomeronasal’ projections from the accessory olfactory bulb and ‘olfactory’ projections from the main bulb, revealed that rostral CMA lesions which damaged the medial nucleus and extended to the ventral surface of the brain (ventral lesions) interrupted vomeronasal input to the more caudally-placed posteromedial cortical nucleus, but spared olfactory inputs to adjacent caidal areas of the amygdala and piriform lobe. In contrast, lesions which damaged a major portion of the medial nucleus but left its ventral surface intact (dorsal lesions) spared both vomeronasal and olfactory inputs to more caudal areas. Animals with both dorsal and ventral lesions failed to mate posteperatively, whereas animals bearing sham lesions of basolateral amygdaloid lesions, which, like dorsal lesions, spared caudally-directed chemosensory afferents, continued to mate normally. We conclude that mating deficits seen after rostral CMA lesions are due primarily to destruction of the medial nucleus.     

Projections of olfactory bulbs to the olfactory and vomeronasal cortices

Projections from the olfactory bulbs have been traditionally described as 'nontopographically organized'. Olfactory and vomeronasal projections have been reported to reach nonoverlapping cortical areas. Four receptor expression zones have been described in the olfactory epithelium, maintained in the main olfactory bulb, but none in the olfactory cortex. Recent data have demonstrated convergence in the basal telencephalon of olfactory and vomeronasal projections. Injections of methanesulfonate hydroxystilbamidine (FluoroGold) in the chemosensory cortex were done to map retrograde labeling in the bulbs. Topography was not observed in the four zones of the main olfactory bulb. Areas of the rostral telencephalon were shown to receive simultaneous inputs from the main and accessory olfactory bulbs.     

Afferent and efferent connections of the olfactory bulbs in the lizard Podarcis hispanica.

The connections of the olfactory bulbs of Podarcis hispanica were studied by tract-tracing of injected horseradish peroxidase. Restricted injections into the main olfactory bulb (MOB) resulted in bilateral terminallike labeling in the medial part of the anterior olfactory nucleus (AON) and in the rostral septum, lateral cortex, nucleus of the lateral olfactory tract, and ventrolateral amygdaloid nucleus. Bilateral retrograde labeling was found in the rostral lateral cortex and in the medial and dorsolateral AON. Ipsilaterally the dorsal cortex, nucleus of the diagonal band, lateral preoptic area, and dorsolateral amygdala showed labeled cell bodies. Retrogradely labeled cells were also found in the midbrain raphe nucleus. Results from injections into the rostral lateral cortex and lateral olfactory tract indicate that the mitral cells are the origin of the centripetal projections of the MOB. Injections in the accessory olfactory bulb (AOB) produced ipsilateral terminallike labeling of the ventral AON, bed nucleus of the accessory olfactory tract, central and ventromedial amygdaloid nuclei, medial part of the bed nucleus of the stria terminalis, and nucleus sphericus. Retrograde labeling of neurons was observed ipsilaterally in the bed nucleus of the accessory olfactory tract and stria terminalis, in the central amygdaloid nucleus, dorsal cortex, and nucleus of the diagonal band. Bilateral labeling of somata was found in the ventral AON, the nucleus sphericus (hilus), and in the mesencephalic raphe nucleus and locus coeruleus. Injections into the dorsal amygdala showed that the mitral neurons are the cells of origin of the AOB centripetal projections. Reciprocal connections are present between AOB and MOB. To our knowledge, this is the first study to address the afferent connections of the olfactory bulbs in a reptile. On the basis of the available data, a discussion is provided of the similarities and differences between the reptilian and mammalian olfactory systems, as well as of the possible functional role of the main olfactory connections in reptiles.     

Efferents and centrifugal afferents of the main and accessory olfactory bulbs in the hamster

The efferents and centrifugal afferents of the hamster olfactory bulbs were studied using orthograde and retrograde tracing techniques. Following injections of tritiated amino acids which were restricted to the main olfactory bulb (MOB), autoradiographic grains were observed ipsilaterally over layer IA of the entire anterior olfactory nucleus (AON), the ventral portion of the hippocampal rudiment (HR), the entire prepyriform cortex and olfactory tubercle, the anterior and posterolateral cortical amygdaloid nuclei and the lateral entorhinal cortex. An ipsilateral projection to the nucleus of the lateral olfactory tract (nLOT) was also indicated. No subcortical or contralateral projections were observed. Amino acid injections into the accessory olfactory bulb (AOB) revealed ipsilateral projections to the superficial plexiform layer of the medial and posteromedial cortical amygdaloid nuclei and to the bed nucleus of the accessory olfactory tract (nAOT) and the bed nucleus of the stria terminalis (nST). Following injections of HRP which were restricted to the MOB, contralateral HRP-positive neurons were found predominantly in pars externa and to a lesser extent in the other subdivisions of the AON. Centrifugal projections to the MOB were identified ipsilaterally from the entire AON, the ventral portion of the HR, the anterior portion of the prepyriform cortex, and the nLOT. No labelled neurons were found in the olfactory tubercle, the anterior and posterolateral cortical amygdaloid nuclei or the entorhinal cortex. Centrifugal projections to the MOB were also identified from subcortical structures of the ipsilateral basal forebrain and from midline structures of the midbrain. Labelling occurred in the fusiform neurons of the diagonal band near the medial base of the forebrain at the level of caudal olfactory tubercle. Heavy labelling was seen in a distinct group of large, predominantly multipolar neurons (magnocellular preoptic area) that continued from the level of caudal olfactory tubercle to the level of the nLOT. This band of HRP-positive neurons could be followed more caudally to a position dorsal and medial to the nLOT near the lateral margin of the lateral anterior hypothalamic area. The midbrain projections to the MOB originated in the dorsal and median raphe nuclei. After injections of HRP into the AOB, centrifugal projections were identified from the nAOT and the posteromedial cortical amygdaloid nucleus. In addition, isolated neurons were labelled in the medial cortical amygdaloid nucleus but no labelled neurons were found in the nST. These results support the notion of two anatomically distinct olfactory systems and demonstrate two previously unreported pathways through which the limbic system may modulate sensory processing in the olfactory bulb.     

Morphology and axonal projection pattern of neurons in the telencephalon of the fire-bellied toad Bombina orientalis: an anterograde, retrograde, and intracellular biocytin labeling study

The connectivity and cytoarchitecture of telencephalic centers except dorsal and medial pallium were studied in the fire-bellied toad Bombina orientalis by anterograde and retrograde biocytin labeling and intracellular biocytin injection (total of 148 intracellularly labeled neurons or neuron clusters). Our findings suggest the following telencephalic divisions: (1) a central amygdala-bed nucleus of the stria terminalis in the caudal midventral telencephalon, connected to visceral-autonomic centers; (2) a vomeronasal amygdala in the caudolateral ventral telencephalon receiving input from the accessory olfactory bulb and projecting mainly to the preoptic region/hypothalamus; (3) an olfactory amygdala in the caudal pole of the telencephalon lateral to the vomeronasal amygdala receiving input from the main olfactory bulb and projecting to the hypothalamus; (4) a medial amygdala receiving input from the anterior dorsal thalamus and projecting to the medial pallium, septum, and hypothalamus; (5) a ventromedial column formed by a nucleus accumbens and a ventral pallidum projecting to the central amygdala, hypothalamus, and posterior tubercle; (6) a lateral column constituting the dorsal striatum proper rostrally and the dorsal pallidum caudally, and a ventrolateral column constituting the ventral striatum. We conclude that the caudal mediolateral complex consisting of the extended central, vomeronasal, and olfactory amygdala of anurans represents the ancestral condition of the amygdaloid complex. During the evolution of the mammalian telencephalon this complex was shifted medially and involuted. The mammalian basolateral amygdala apparently is an evolutionary new structure, but the medial portion of the amygdalar complex of anurans reveals similarities in input and output with this structure and may serve similar functions.     

Differential projections of the anterior and posterior regions of the medial amygdaloid nucleus in the Syrian hamster.

The medial nucleus of the amygdala is important for the neural control of reproductive behavior in the adult male Syrian hamster. Two types of signals are essential for this behavior, chemosensory stimuli and gonadal steroids; these signals appear to be received in different parts of the medial nucleus. The anterior region receives input from olfactory and vomeronasal systems, both of which are required for this behavior, whereas the posterior region receives gonadal hormone inputs. Behavioral studies have also suggested a functional differentiation of these two areas; electrolytic lesions of the anterior, but not the posterior, part eliminates normal sexual behavior. In this study, the efferent projections of the anterior and posterior divisions of the medial nucleus of the amygdala in the Syrian hamster were analyzed throughout the forebrain after injections of the anterograde neuronal tracer, Phaseolus vulgaris-leucoagglutinin. Neurons of the anterior, but not the posterior, medial nucleus, were found to project to numerous olfactory bulb projection areas and to the ventral striatopallidal complex. Within areas of the chemosensory circuitry that control reproductive behavior, the anterior region of the medial nucleus projects to the intermediate part of the posterior bed nucleus of the stria terminalis and the lateral part of the medial preoptic area, whereas the posterior region of the medial nucleus projects to the medial parts of these areas. Differences in targets were also observed in the ventromedial nucleus of the hypothalamus where the anterior region projects to the core while the posterior part projects to the shell of this nucleus. Furthermore, reciprocal projections between the anterior and posterior regions of the medial nucleus were observed. Taken together, these studies support the hypothesis that the anterior and posterior regions of the medial amygdaloid nucleus provide substantially different contributions to the control of reproductive behaviors.     

V1R and V2R segregated vomeronasal pathways to the hypothalamus

The vomeronasal system is segregated from the epithelium to the bulb. Two classes of receptor neurons are apically and basally placed in the vomeronasal epithelium, express Gi2alpha and Goalpha proteins and V1R and V2R receptors and project to the anterior and posterior portions of the accessory olfactory bulb, respectively. Apart from common vomeronasal recipient structures in the amygdala, only the anterior accessory olfactory bulb projects to the bed nucleus of the stria terminalis and only the posterior accessory olfactory bulb projects to the dorsal anterior amygdala. The efferent projections from these two amygdaloid structures to the hypothalamus were investigated. These two vomeronasal subsystems mediated by V1R and V2R receptors were partially segregated, not only in amygdala, but also in the hypothalamus.     

Amygdaloid efferents through the stria terminalis in the rat give origin to zinc-containing boutons

Many regions of the basal forebrain are innervated by zinc-containing axonal boutons. In the present work, the lesion/degeneration method, coupled with histochemical staining for zinc-containing boutons, was used to determine the origins and efferent pathways of these zinc-containing projections to the basal forebrain. Knife cuts of the stria terminalis or extensive electrolytic lesions of the amygdala resulted in the bleaching of the staining for zinc (Timm stain) and terminal degeneration (Fink-Heimer method) ipsilaterally in the following areas: granule cell layer of the accessory olfactory bulb, shell of nucleus accumbens, bed nucleus of the stria terminalis, striohypothalamic nucleus, retrochiasmatic area, ventromedial hypothalamic nucleus (in the cell-sparse shell), medial tuberal nucleus, terete hypothalamic nucleus, and ventral premammillary nucleus. Small lesions made with ibotenic acid in the posteromedial part of the amygdalohippocampal area caused bleaching of the stain for zinc in the accessory olfactory bulb, in the medial zone of the bed nucleus of the stria terminalis, and in the ventral premammillary nucleus. Lesions in either the ventral subiculum or the anterolateral part of the amygdalohippocampal area caused bleaching in the ventromedial hypothalamic nucleus. Lesions in the hippocampus or in the neocortex did not produce bleaching of the stain for zinc in the above-mentioned terminal fields. The present results agree with previous studies on amygdaloid efferents and suggest that neurons in the amygdalohippocampal area and, possibly, in the ventral subiculum give origin to zinc-containing boutons.     

Neural substrates for processing chemosensory information in snakes

Snakes interact with their chemical environment through their olfactory and vomeronasal systems. The present report summarizes advances on neural substrates for processing chemosensory information. First, the efferent and centrifugal afferent connections of the main and accessory olfactory bulbs were reinvestigated. Second, the afferent and efferent connections of the nucleus sphericus, the main target of the accessory olfactory bulb, were characterized. The nucleus sphericus gives rise to a very small projection to the hypothalamus, but it does project to other telencephalic structures where olfactory and vomeronasal information could converge. Third, the intra-amygdaloid circuitry and the amygdalo-hypothalamic projections were described. The medial amygdala, for instance, receives both vomeronasal and olfactory inputs and projects to the hypothalamus, namely, to the lateral posterior hypothalamic nucleus. Fourth, because the lateral posterior hypothalamic nucleus projects to the hypoglossal nucleus, the motor center controlling the tongue musculature, this projection could constitute a pathway for chemosensory information to influence tongue-flicking behavior. In summary, vomeronasal information is mostly relayed to the hypothalamus not via the nucleus sphericus but through other telencephalic structures. Convergence of olfactory and vomeronasal information appears to occur at different levels in the telencephalon. A neural substrate for the chemosensory control of tongue-flicking behavior is provided.     

Experience facilitates vomeronasal and olfactory influence on Fos expression in medial preoptic area during pheromone exposure or mating in male hamsters

Chemosensory stimuli are essential for mating in male hamsters but either main olfactory or vomeronasal input is sufficient in sexually experienced males. Activation in central chemosensory pathways and medial preoptic area, after stimulation with female chemosignals or after mating, was estimated by counting neurons expressing Fos protein in experienced and naive males, with or without vomeronasal organ lesions. Regions counted included main and accessory olfactory bulbs, corticomedial amygdala, bed nucleus stria terminalis and medial preoptic area. Chemosensory stimulation was more effective in activating medial preoptic area in experienced than in naive males. In experienced males with vomeronasal organs removed, main olfactory input was as effective in activating medial preoptic area as was the combination of main and accessory input available to intact animals. As previously reported, the main olfactory input remaining after vomeronasal lesions in naive males was poorly effective in activating medial preoptic area, and these animals had impaired mating behavior. The change in access of chemosensory input to medial preoptic area after experience suggests that an experience-dependent synaptic modulation in this pathway, perhaps in the amygdala, may underlie some changes in mating behavior with experience.     

Hodological characterization of the medial amygdala in anuran amphibians

Early studies in anuran amphibians defined the amygdala as a single unit that only later could be subdivided into medial and lateral parts with the achievement of sensitive immunohistochemical and tracing techniques. However, the terminology used was often misleading when comparing with "homologous" amygdaloid nuclei in amniotes. Recently, the basal telencephalon of anurans has been demonstrated to be more complex than previously thought, and distinct amygdaloid nuclei were proposed on the basis of immunohistochemistry. Moreover, developmental data are increasing that support this notion. In the present study, we analyzed the patterns of afferent and efferent connections of the medial amygdala (MeA; formerly amygdala pars lateralis), considered as the main target of the vomeronasal information from the accessory olfactory bulb, as in other vertebrates. By means of axonal transport of dextran amines, the afferent and efferent connections of the MeA were traced in Rana perezi and Xenopus laevis under in vivo and in vitro conditions. Largely similar results were found in both species. The results showed abundant intratelencephalic and extratelencephalic connections that were readily comparable to those of other tetrapods. Most of these connections were reciprocal and, in particular, the strong relation of the MeA with the hypothalamus, via the stria terminalis, was demonstrated. Immunohistochemical techniques showed staining patterns that revealed abundant peptidergic afferents to the MeA, as well as minor inputs containing other neurotransmitters such as catecholamines. Double-labeling experiments demonstrated that the peptidergic fibers that reach the MeA originate in the ventral hypothalamus, whereas the catecholaminergic innervation of the MeA arises in the caudal extent of the posterior tubercle. Taken together, the results about connectivity in our study support the comparison of the MeA in anurans with its counterparts (and similarly named) amygdaloid nuclei in amniotes. Most of the hodological features of the medial amygdala seem to be shared by those tetrapods with well-developed vomeronasal systems.     

The accessory olfactory bulbs and the lateral telencephalic wall of the rat-fish, Chimaera

The lateral telencephalon of Chimaera possesses several unique features but also has nuclei and fiber systems homologous with those of other sub-mammalian vertebrates. Ventricular ridges, similar to those of reptiles, are quite evident. Accessory olfactory bulbs are associated with the dorsal and ventral parts of each olfactory bulb. These contribute to the lateral olfactory tract. The internal granular layer caudal to the olfactory and the accessory bulbs blends with the anterior olfactory nucleus. Caudal to this nuclear area, the nuclei of the rostral telencephalon are well differentiated. Nuclear areas distinguishable in the lateral hemisphere include: the primordial dorsal pallium, the primordial piriform cortex, the primordial striatal and amygdaloid nuclei, and the lateral zone of the olfactory tubercle. These areas replace dorsal, dorsolateral, ventrolateral and ventral parts of the anterior olfactory nucleus, respectively. The primordial striatum is subdivided into hyperstriatum, neostriatum, paleostriatum augmentatum and paleostriatum primitivum. The amygdaloid area has anterior, corticomedial and basolateral nuclear groups. The basolateral area is best differentiated. The hyperstriatum forms a rostral ventricular eminence; the basolateral amygdaloid nucleus is present in a larger caudal ventricular ridge. Fiber tracts of the lateral wall include the lateral olfactory tract, the lateral corticohabenular tract, the lateral forebrain bundle and the stria terminalis. Nuclei of medial and lateral walls are interrelated through the hippocampal and the anterior commissures.     

Amygdalo-hypothalamic projections in the lizard Podarcis hispanica: A combined anterograde and retrograde tracing study

The cells of origin and terminal fields of the amygdalo-hypothalamic projections in the lizard Podarcis hispanica were determined by using the anterograde and retrograde transport of the tracers, biotinylated dextran amine and horseradish peroxidase. The resulting labeling indicated that there was a small projection to the preoptic hypothalamus, that arose from the vomeronasal amygdaloid nuclei (nucleus sphericus and nucleus of the accessory olfactory tract), and an important projection to the rest of the hypothalamus, that was formed by three components: medial, lateral, and ventral. The medial projection originated mainly in the dorsal amygdaloid division (posterior dorsal ventricular ridge and lateral amygdala) and also in the centromedial amygdaloid division (medial amygdala and bed nucleus of the stria terminalis). It coursed through the stria terminalis and reached mainly the retrochiasmatic area and the ventromedial hypothalamic nucleus. The lateral projection originated in the cortical amygdaloid division (ventral anterior and ventral posterior amygdala). It coursed via the lateral amygdalofugal tract and terminated in the lateral hypothalamic area and the lateral tuberomammillary area. The ventral projection originated in the centromedial amygdaloid division (in the striato-amygdaloid transition area), coursed through the ventral peduncle of the lateral forebrain bundle, and reached the lateral posterior hypothalamic nucleus, continuing caudally to the hindbrain. Such a pattern of the amygdalo-hypothalamic projections has not been described before, and its functional implications in the transfer of multisensory information to the hypothalamus are discussed. The possible homologies with the amygdalo-hypothalamic projections in mammals and other vertebrates are also considered. J. Comp. Neurol. 384:537–555, 1997. © 1997 Wiley-Liss, Inc.     

Connectivity and cytoarchitecture of telencephalic centers in the fire-bellied toad Bombina orientalis

In the fire-bellied toad Bombina orientalis, the connectivity and cytoarchitecture of telencephalic structures were studied by intracellular, anterograde and retrograde biocytin labelling in order to elucidate the neuronal basis of fear conditioning and context learning in amphibians. Our findings suggest the existence of a central amygdala-bed nucleus of the stria terminalis complex in the caudal mid-ventral telencephalon, a vomeronasal amygdala in the caudolateral ventral telencephalon, an olfactory amygdala in the caudal pole of the telencephalon lateral of the vomeronasal amygdala, and a ventromedially situated "medial" amygdala, which is assumed to be functionally equivalent to the basolateral amygdala of mammals. A ventromedial cellular column forms a nucleus accumbens rostrally and continues caudally into a shell-like ventral pallidum. A lateral column constitutes a dorsal striatum proper rostrally, a dorsal pallidum caudally, and a mixed striato-pallidum at intermediate levels. We conclude that the caudal mediolateral complex consisting of an extended central, vomeronasal and olfactory amygdala of anurans represents the ancestral equivalent of the amygdaloid complex of tetrapods. During the evolution of the mammalian telencephalon, this complex apparently was shifted medially and involuted.     

Thalamoamygdaloid projections in the rat: a test of the amygdala's role in sensory processing.

We used the autoradiographic tract-tracing method to define the amygdaloid projection fields after injecting 3H-amino acids into individual thalamic nuclei in the rat. The parvicellular division of the ventroposterior nucleus, the thalamic taste relay, projected lightly to the central and lateral amygdaloid nuclei. The central medial, interanteromedial, and paraventricular thalamic nuclei, viscerosensory relays of the thorax and abdomen, projected heavily to the amygdala. All projected to the basolateral amygdaloid nucleus, the paraventricular nucleus in addition having terminations in the central nucleus, the amygdaloid portion of the nucleus of the stria terminalis, and the amygdalohippocampal transition area. The magnocellular division of the medial geniculate, a thalamic auditory (and, to a moderate degree, a spinothalamic) relay, sent heavy projections to the central, accessory basal, lateral, and anterior cortical nuclei, and to the anterior amygdaloid area and the nucleus of the accessory olfactory tract. Other thalamic nuclei projecting to the amygdala, for which functions could not be associated, were the paratenial and subparafascicular nuclei. The former projected to the lateral, basal, and posterolateral cortical nuclei; the latter projected very lightly to the central, medial, and basal accessory nuclei. These results show that, like the cortical amygdaloid nuclei, which are sensory (olfactory) in nature, the subcortical amygdaloid nuclei must have major sensory functions. These thalamic afferents, when correlated with cortical and brainstem data from the literature, suggested that the amygdala is in receipt of sensory information from many modalities. To uncover the manner by which such information is processed by the amygdala and relayed to effector areas of the brain, six hypothetical mechanisms relating to modality specificity and convergence were posited. By charting sensory-related afferents to all subdivisions of the amygdala, each nucleus was characterized as to its mechanism of information processing. Four proposed amygdaloid systems emerged from this analysis. A unimodal corticomedial amygdaloid system relays pheromonal information from the accessory olfactory bulb to medial basal forebrain and hypothalamic areas. A second system--the lateral-basomedial--collects and combines input from a number of sensory modalities and distributes it to the same basal forebrain and hypothalamic areas as the corticomedial. The central system appears to concentrate the effect of viscerosensory information arriving from multiple brainstem, thalamic, cortical, and amygdaloid sources; this information is combined with significant auditory and spinothalamic inputs from the thalamus and cortex. The central system projects to lateral nuclei in the basal forebrain, hypothalamus, and brainstem.(ABSTRACT TRUNCATED AT 400 WORDS)     

Afferent connections to the amygdaloid complex of the rat and cat: II. Afferents from the hypothalamus and the basal telencephalon

The projections from the basal telencephalon and hypothalamus to each nucleus of the amygdaloid complex of the rat, and to the central amygdala of the cat, were investigated by the use of retrograde transport of horseradish peroxidase (HRP). The enzyme was injected stereotaxically by microiontophoresis, using three different approaches. The ventral pallidum (Heimer, '78) and ventral part of the globus pallidus were found to project to the lateral and basolateral nuclei of the amygdala. The substantia innominata projects diffusely to the entire amygdaloid complex, except to the lateral nucleus and the caudal part of the medial nucleus. The anterior amygdaloid area shows a similar projection field, the only difference being that this structure does not project to any parts of the medial nucleus. The dorsal subdivision of the nucleus of the lateral olfactory tract sends fibers to the ipsilateral as well as the contralateral basolateral nucleus, and possibly to the ipsilateral basomedial and cortical amygdala. The ventral subdivision of the nucleus of the lateral olfactory tract was massively labeled after an injection in the ipsilateral central nucleus, but this injection affected the commissural component of the stria terminalis. The nucleus of the horizontal limb of the diagonal band of Broca connects with the medial, central, and anterior cortical nuclei, whereas the bed nucleus of stria terminalis and medial preoptic area are related to the medial nucleus predominantly. The lateral preoptic area is only weakly labeled after intra-amygdaloid HRP injections. The hypothalamo-amygdaloid projections terminate preponderantly in the medial part of the amygdaloid complex. Thus, axons from neurons in the area dorsal and medial to the paraventricular nucleus of the hypothalamus distribute to the medial nucleus and intra-amygdaloid part of the bed nucleus of stria terminalis. Most of the amygdalopetal fibers from the ventromedial, ventral premammillary, and arcuate nuclei of the hypothalamus end in the medial nucleus, but some extend into the central nucleus. A few fibers from the ventromedial nucleus of the hypothalamus reach the basolateral nucleus. The lateral hypothalamic area projects heavily to the central nucleus, and more sparsely to the medial and basolateral nuclei. The dorsal hypothalamic area and supramammillary nucleus show restricted projections to the central and basolateral nuclei, respectively. There are only a modest number of crossed hypothalamo-amygdaloid fibers. Most of these originate in the ventromedial nucleus of the hypothalamus and terminate in the contralateral medial nucleus. The projections from the basal telencephalon and hypothalamus to the central nucleus of the amygdala of the cat are similar to the corresponding projections in the rat.     

Adjacent laminar terminations of two centrifugal afferent pathways to the accessory olfactory bulb in the mouse

Anterograde and retrograde axonal tracing methods have been combined with transection of the stria terminalis to investigate the centrifugal afferent connections of the accessory olfactory bulb in the mouse.Injection of tritiated proline into the postero-medial cortical amygdaloid nucleus (C₃) gives rise to anterograde autoradiographic labelling of a pathway terminating in the internal granular layer of the accessory olfactory bulb (AOB). Transection of the ipsilateral stria terminalis completely abolishes labelling of this pathway. Injections further rostral, in the bed nucleus of the accessory olfactory tract (bnAOT) and medial amygdaloid nucleus (M), give rise to labelling of a second ipsilateral afferent pathway to the AOB which terminates in the internal plexiform layer (IPL) and is unaffected by strial transection.Injections of wheat germ lectin-HRP conjugate into the AOB confirm that it receives afferents from the ipsilateral bnAOT, M and C₃, and from a few cells in the contralateral C₃. Transection of the ipsilateral stria terminalis prevents retrograde labelling of any cells in the ipsilateral C₃, but does not affect labelling of cells in M or bnAOT (or contralateral C₃). The conjugate is also transported anterogradely in this system, labelling the efferent projections of the AOB to bnAOT, M and C₃.It is concluded that the AOB receives at least two sets of ipsilateral afferents: one set from C₃, via the stria terminalis, terminating in the internal granular layer, and a second set from M and/or bnAOT terminating in the IPL and probably running in the accessory olfactory tract.