Parvalbumin is expressed in a reciprocal circuit linking the medial geniculate body and auditory neocortex in the rabbit

Recent studies of the rabbit auditory forebrain have shown that antibodies directed against the calcium-binding protein parvalbumin (PV) specifically demarcate auditory neocortex and the ventral division of the medial geniculate body (MGV). The auditory cortex is characterized by two PV- immunoreactive bands: dense terminal-like labeling within layer III/IV and a prominent band of PV+ somata in the upper half of layer VI. In some cases, there are distinct patches of PV immunoreactivity within layers III/IV of auditory cortex that appear similar to the patchy termination of thalamocortical axons labeled by the injection of anterograde tracers into MGV. The presence of PV+ patches in III/IV, PV+ somata in layer VI, and the high density of PV+ neurons and terminals in the MGV suggest the existence of a reciprocal PV+ circuit linking primary auditory cortex (AI) and the MGV. In the present study, double-labeling experiments in adult rabbits were carried out to provide evidence for this circuit. Focal injections of the tracers biocytin or biotinylated dextran amine (BDA) into the MGV labeled thalamocortical afferent patches within layer III/IV and retrogradely labeled corticothalamic neurons in layer VIa of the ipsilateral auditory cortex. Adjacent sections stained with antibodies against PV revealed terminal-like PV-immunoreactive patches in III/IV and PV+ somata in VIa that were in register with those labeled by BDA injections into the MGV. Serial section reconstruction of BDA-labeled corticothalamic neurons in VIa revealed pyramidal cells with tangentially oriented basal dendrites and sparsely branched apical dendrites that ascended to layer I. Fluorescent double-labeling studies demonstrated that a subpopulation of corticothalamic neurons also express PV. PV-negative corticothalamic neurons were also found. Discrete injections of BDA into auditory cortex labeled bands of neurons in the ipsilateral MGV, whose orientation paralleled the fibrodendritic laminae characteristic of this subdivision. Retrograde double-labeling experiments showed that most MGV relay neurons also express PV. Small numbers of PV-negative relay neurons were also found. These studies provide evidence for the existence of multiple, chemically coded pathways linking primary auditory cortex and the MGV. J. Comp. Neurol. 400:349–362, 1998. © 1998 Wiley-Liss, Inc.     

Plasticity in the tonotopic organization of the medial geniculate body in adult cats following restricted unilateral cochlear lesions

To investigate subcortical contributions to cortical reorganization, the frequency organization of the ventral nucleus of the medial geniculate body (MGv) in six normal adult cats and in eight cats with restricted unilateral cochlear lesions was investigated using multiunit electrophysiological recording techniques. The tonotopic organization of MGv in the lesioned animals, with severe mid-to-high frequency hearing losses, was investigated 40-186 days following the lesioning procedure. Frequency maps were generated from neural responses to pure tone bursts presented separately to each ear under barbiturate anesthesia. Consideration of the frequency organization in normal animals, and of the apparently normal representation of the ipsilateral (unlesioned) cochlea in lesioned animals, allowed for a detailed specification of the extent of changes observed in MGv. In the lesioned animals it was found that, in the region of MGv in which mid-to-high frequencies are normally represented, there was an "expanded representation" of lesion-edge frequencies. Neuron clusters within these regions of enlarged representation that had "new" characteristic frequencies displayed response properties (latency, bandwidth) very similar to those in normal animals. Thresholds of these neurons were not consistent with the argument that the changes merely reflect the residue of prelesion responses, suggesting a dynamic process of reorganization. The tonotopic reorganization observed in MGv is similar to that seen in the primary auditory cortex and is more extensive than the reorganization found in the auditory midbrain, suggesting that the auditory thalamus plays an important role in cortical plasticity.     

Cell types and response properties of neurons in the ventral division of the medial geniculate body of the rabbit

Although there is evidence for multiple classes of thalamic relay neurons in the auditory thalamus, correlative anatomical and physiological studies are lacking. We have used the juxtacellular labeling technique, in conjunction with Nissl, Golgi, and immunocytochemical methods, to study the morphology and response properties of cells in the ventral division of the medial geniculate body of the rabbit. Single units in the ventral division of the medial geniculate body (MGV) were characterized extracellularly with monaural and binaural tone and noise bursts (100- to 250-msec duration). Characterized units were filled with biocytin and visualized with an antibody enhanced diaminobenzidine reaction. A total of 31 neurons were physiologically characterized and labeled with the juxtacellular technique. Labeled neurons were fully reconstructed from serial sections by using a computer microscope system. Three subregions of the rabbit MGV were identified, each characterized by differences in Nissl architecture, calcium-binding protein expression, and by the dendritic orientation of tufted relay neurons. In general, the dendritic fields of relay neurons were closely aligned with the cellular laminae. Qualitative and quantitative analyses revealed two types of presumptive relay neurons within the MGV. Type I cells had thick dendrites with a greater total volume and morphologically diverse appendages compared with the Type II cells whose dendrites were thin with a moderate number of small spines. Both classes were acoustically responsive and exhibited a variety of response patterns, including onset, offset, and sustained responses. In terms of binaural characteristics, most (ca. 53%) labeled neurons were of the EE type, with the remaining cells classified as EO (27%) or EI (20%) response types. Two types of presumptive interneurons were also seen: bipolar neurons with large dendritic fields and a small neurogliaform variety. Cell types and dendritic orientation within the MGV are discussed in terms of the physiological organization of the rabbit auditory thalamus.     

The neuronal architecture of the dorsal division of the medial geniculate body of the cat. A study with the rapid Golgi method

The neurons in the nuclei of the dorsal division of the medial geniculate body were studied with the rapid Golgi method in kittens and young adult cats. The dorsal nuclei contain two principal cell types: a large stellate neuron with radiate dendrites and a bushy neuron with tufted dendrites, each with extensive dendritic fields. Two sizes of cells with locally arborizing axons (local circuit neurons) were found. The small and commonly observed one is stellate in shape, has a limited dendritic domain, and an axon with multiple, often profuse collaterals ending in the vicinity of the cell. A second, and much less common variety (large local circuit neuron) is somewhat larger and has fewer axon collaterals. Subtle, but distinct variations in these cell types distinguish the deep and superficial dorsal nuclei and also the anterior tier of nuclei (deep dorsal and superficial). These functional differences may correlate with the relative morphological homogeneity of the ventral nucleus compared to the extremely heterogeneous medial division. The dorsal division should be regarded as part of the pulvinar-lateralis posterior complex both structurally and functionally. In the suprageniculate nucleus, the principal neurons are stellate cells with large perikarya and numerous and extensive dendrites covered with appendages. The large axon is devoid of collaterals. A small local circuit cell with several axon collaterals, and sparse, restricted dendrites has also been observed. In the adjacent posterior limitans nucleus, the principal neuron has a medium-sized, piriform or somewhat elongated perikaryon, a few very long radiating dendrites, which may span the depth of the nucleus, and a long, poorly branched axon. Small neurons are also seen here. A comparison of the structure, connections, and function of the medial geniculate body suggests that the dorsal division is predominantly, but probably not exclusively auditory, while the ventral nucleus is entirely auditory and relatively homogeneous, and the medial division, polymodal and heterogeneous with respect to input.     

Projections of the amygdala to the thalamus in the cynomolgus monkey

The projections of the amygdala to the thalamus in cynomolgus monkeys (Macaca fascicularis) were studied with both anterograde and retrograde axonal tracing techniques. Horseradish peroxidase (HRP) was injected into medial and midline thalamic sites in five animals, and tritiated amino acids were injected into selected amygdaloid regions in a total of 13 hemispheres in ten animals. The findings from the two types of tracer experiments demonstrated the origins, course, and terminal pattern of amygdaloid projections to two thalamic nuclei--medialis dorsalis (MD) and reuniens. Almost all of the amygdaloid nuclei contribute projections to MD, though the greatest proportion arise from the basal group and terminate in discrete, interlocking patches within the medial, magnocellular portion of MD. In addition to this major projection, the central and medial amygdaloid nuclei send a lighter projection to the lateral portion of nucleus reuniens. The amygdalothalamic projections took a variety of routes out of the amygdala before the large majority joined the inferior thalamic peduncle and entered the rostral head of the thalamus where they turned caudally toward their targets. A small number of amygdalothalamic fibers may also run in the stria terminalis.     

GABAergic circuitry in the dorsal division of the cat medial geniculate nucleus

Gamma-aminobutyric acid (GABA) is the main inhibitory neurotransmitter of the thalamus. We used postembedding immunocytochemistry to examine the synaptic organization of GABA-positive profiles in the dorsal superficial subdivision of the cat medial geniculate nucleus (MGN). Three groups of GABA-positive profiles participate in synapses: axon terminals, dendrites, and presynaptic dendrites. The presynaptic GABA-positive terminals target mainly GABA-negative dendrites. The GABA-positive postsynaptic profiles receive input primarily from GABA-negative axons. The results indicate that the synaptic organization of GABA-positive profiles in the dorsal superficial subdivision of the MGN nucleus is very similar to that in other thalamic nuclei.     

Projections from the medial geniculate body to primary auditory cortex in neonatally deafened cats

In the present study, anatomical projections from the medial geniculate body (MGB) to primary auditory cortex (AI) were investigated in normal adult cats and in animals that were neonatally deafened with the ototoxic drug amikacin. Cochleotopic/tonotopic maps in AI (based on neural response characteristic frequency) were obtained with microelectrode recording techniques, and single or multiple injections of retrograde tracers (horseradish peroxidase and fluorescent dyes) were introduced into AI. The AI maps of the amikacin-treated cats had an abnormal cochleotopic organization, such that deprived cortical areas exhibited an expanded representation of intact regions of the damaged cochlea. However, retrograde tracer injections into different regions of AI produced a normal pattern of labeling in the ventral division of the medial geniculate body (MGBv). In both experimental and control animals, the main mass of labeled thalamic cells was found in the MGBv. Different isofrequency contours in AI receive input from different portions of the MGBv. Thus, cell arrays labeled by anterior AI injections were situated medially in MGBv, and injections into posterior AI labeled MGBv more laterally. Furthermore, the deafened cats did not develop a more divergent thalamocortical projection compared with normal control animals, indicating that an abnormal spread of the thalamocortical afferents across the frequency domain in AI (anterior-posterior axis) is not responsible for the altered cochleotopic map in these neonatally deafened animals. The relatively normal thalamocortical projection pattern suggests that, after neonatal cochlear lesions, the major reorganization of cochleotopic maps occurs at subthalamic levels.     

Projections of auditory cortex to the medial geniculate body of the cat

The corticofugal projection from 12 auditory cortical fields onto the medial geniculate body was investigated in adult cats by using wheat germ agglutinin conjugated to horseradish peroxidase or biotinylated dextran amines. The chief goals were to determine the degree of divergence from single cortical fields, the pattern of convergence from several fields onto a single nucleus, the extent of reciprocal relations between corticothalamic and thalamocortical connections, and to contrast and compare the patterns of auditory corticogeniculate projections with corticofugal input to the inferior colliculus. The main findings were that (1) single areas showed a wide range of divergence, projecting to as few as 5, and to as many as 15, thalamic nuclei; (2) most nuclei received projections from approximately five cortical areas, whereas others were the target of as few as three areas; (3) there was global corticothalamic-thalamocortical reciprocity in every experiment, and there were also significant instances of nonreciprocal projections, with the corticothalamic input often more extensive; (4) the corticothalamic projection was far stronger and more divergent than the corticocollicular projection from the same areas, suggesting that the thalamus and the inferior colliculus receive differential degrees of corticofugal control; (5) cochleotopically organized areas had fewer corticothalamic projections than fields in which tonotopy was not a primary feature; and (6) all corticothalamic projections were topographic, focal, and clustered, indicating that areas with limited cochleotopic organization still have some internal spatial arrangement. The areas with the most divergent corticothalamic projections were polysensory regions in the posterior ectosylvian gyrus. The projection patterns were indistinguishable for the two tracers. These findings suggest that every auditory thalamic nucleus is under some degree of descending control. Many of the projections preserve the relations between cochleotopically organized thalamic and auditory areas, and suggest topographic relations between nontonotopic areas and nuclei. The collective size of the corticothalamic system suggests that both lemniscal and extralemniscal auditory thalamic nuclei receive significant corticofugal input.     

Projections from the amygdalo-piriform transition area to the amygdaloid complex: a PHA-l study in rat

The amygdalo-piriform transition area is a poorly defined region in the temporal lobe that is heavily connected with the olfactory system. As part of an ongoing project aimed at understanding the neuronal pathways that provide sensory information to the amygdala, we investigated the cytoarchitectonic and chemoarchitectonic features of the amygdalo-piriform transition area and its connections to the amygdaloid complex in 13 rats by using the anterograde tracer, Phaseolus vulgaris-leucoagglutinin. Our analysis indicates that the amygdalo-piriform transition area has medial (rostral and caudal portions) and lateral parts. The rostromedial part projects heavily to the intermediate and lateral divisions of the central nucleus, whereas the caudomedial part projects mainly to the medial division. The lateral part of the amygdalo-piriform transition area projects heavily to the capsular and lateral divisions of the central nucleus. Electron microscopic analysis revealed that the projection to the lateral division of the central nucleus forms asymmetric contacts with the spines and shafts of postsynaptic neurons and, therefore, is assumed to be excitatory. The amygdalo-piriform transition area also projects moderately to other amygdaloid nuclei, including the parvicellular division of the basal nucleus, the anterior cortical nucleus, and the nucleus of the lateral olfactory tract. The lateral and medial parts of the amygdalo-piriform transition area also project to the distal temporal CA1 and distal temporal subiculum, respectively. Unlike the adjacent entorhinal cortex, the amygdalo-piriform transition area does not project to the dentate gyrus. These data suggest that the amygdalo-piriform transition area is a region that influences both emotional and memory processing in parallel by means of pathways to the amygdala and the hippocampus, respectively.     

Direct projections from the non-laminated divisions of the medial geniculate nucleus to the temporal polar cortex and amygdala in the cat

The medial geniculate nucleus (MG) is well known to send projection fibers not only to the auditory cortex, but also to the limbic structures of the forebrain including the perirhinal cortex and amygdala. In the cat, the non-laminated portions of the MG are also known to project to the amygdala, as well as to the auditory cortical areas surrounding the primary auditory area. On the other hand, projections from the non-laminated MG to the limbic cortical areas have not so far been studied systematically. Thus, in the present study, direct projections from the non-laminated portions of the medial geniculate nucleus to the temporal polar cortex and amygdala were examined in the cat by retrograde and anterograde tract-tracing techniques. The temporal polar cortex is the ventral polar region of the posterior sylvian and posterior ectosylvian gyri, which is located dorsal to the posterior rhinal sulcus and includes the ectorhinal area. After injection of cholera toxin B subunit into the temporal polar cortex, retrogradely labeled neurons were seen in the caudal two-thirds of the medial geniculate nucleus ipsilateral to the injection; they were distributed in the non-laminated portions of the MG (the dorsal and medial divisions and the ventromedial part of the ventral division), but not in the laminated portion (the principal part of the ventral division). These findings were confirmed by injecting Phaseolus vulgaris leucoagglutinin into each division of the MG. After the injection into each non-laminated division, terminal labeling was observed in the temporal polar cortex. Terminal labeling was further found in the lateral amygdaloid nucleus ipsilateral to the injection. Then, cholera toxin B subunit was injected into the lateral amygdaloid nucleus; retrogradely labeled neurons were observed ipsilaterally in the non-laminated portions of the MG, as well as in the temporal polar cortex. The results indicate that the non-laminated portions of the MG send projection fibers to the temporal polar cortex and lateral amygdaloid nucleus, and that the non-laminated portions of the MG and temporal polar cortex give rise to overlapping projections to the lateral amygdaloid nucleus. These connections appear to constitute neuronal links in “emotional” and/or “motivational” circuitry in the forebrain. © Wiley-Liss, Inc.     

Projections from the amygdaloid complex to the claustrum and the endopiriform nucleus: a Phaseolus vulgaris leucoagglutinin study in the rat

The claustrum and the endopiriform nucleus contribute to the spread of epileptiform activity from the amygdala to other brain areas. Data of the distribution of pathways underlying the information flow between these regions are, however, incomplete and controversial. To investigate the projections from the amygdala to the claustrum and the endopiriform nucleus, we injected the anterograde tracer Phaseolus vulgaris leucoagglutinin into various divisions of the amygdaloid complex, including the lateral, basal, accessory basal, central, anterior cortical and posterior cortical nuclei, the periamygdaloid cortex, and the amygdalohippocampal area in the rat. Analysis of immunohistochemically processed sections reveal that the heaviest projections to the claustrum originate in the magnocellular division of the basal nucleus. The projection is moderate in density and mainly terminates in the dorsal aspect of the anterior part of the claustrum. Light projections from the parvicellular and intermediate divisions of the basal nucleus terminate in the same region, whereas light projections from the accessory basal nucleus and the lateral division of the amygdalohippocampal area innervate the caudal part of the claustrum. The most substantial projections from the amygdala to the endopiriform nucleus originate in the lateral division of the amygdalohippocampal area. These projections terminate in the central and caudal parts of the endopiriform nucleus. Lighter projections originate in the anterior and posterior cortical nuclei, the periamygdaloid cortex, the medial division of the amygdalohippocampal area, and the accessory basal nucleus. These data provide an anatomic basis for recent functional studies demonstrating that the claustrum and the endopiriform nucleus are strategically located to synchronize and spread epileptiform activity from the amygdala to the other brain regions. These topographically organized pathways also provide a route by means of which the claustrum and the endopiriform nucleus have access to inputs from the amygdaloid networks that process emotionally significant information.     

Binaural response patterns in subdivisions of the medial geniculate body

Auditory evoked potentials (AEPs) to binaural click stimulation were examined in the ventral (MGv) and caudomedial (MGcm) subdivisions of the medial geniculate body (MG) in guinea pigs. Binaural stimulation caused a decrease in amplitude for the response component recorded from the MGv, but an increase in amplitude for the AEP component recorded from the MGcm. Findings suggest that the evoked responses recorded from MGv and MGcm are functionally distinct. The inhibitory binaural response (BR) pattern seen in MGv was similar to that of the middle latency response (MLR) component recorded over the temporal cortex, while the additive BR pattern typical of the MGcm was similar to that of the surface midline MLR component. Furthermore, these data imply that the binaural response patterns seen in the primary and non-primary auditory cortex may be processed and encoded at the thalamic level. It is concluded that the distinct BR patterns noted for the two MG subdivisions reflect the predominant type of binaurally responsive neurons within the respective pathways.     

Projections to the medial superior olive from the medial and lateral nuclei of the trapezoid body in rodents and bats.

In this study we present direct evidence of axonal projections from both the medial and lateral nuclei of the trapezoid body to the medial superior olive. Projections were traced by intracellularly labeling cells and axons in a tissue slice preparation of two rodent species, Mus musculus and Meriones unguiculatus and two bat species, Eptesicus fuscus and Pteronotus parnellii. The main axon of most principal cells in the medial nucleus of the trapezoid body gives off one or more collateral branches which arborize within the medial superior olive. These collateral axons form small bouton-like swellings which primarily contact somata within the central cell column in the medial superior olive. Likewise, labeled elongate and multipolar cells of the lateral nucleus of the trapezoid body send axons to both the medial and lateral superior olives. These axons also form perisomatic contacts in both target nuclei. These two sets of projections may relay ascending input to the medial superior olive and the lateral superior olive; the medial nucleus of the trapezoid body is known to relay input from the contralateral ventral cochlear nucleus, and the lateral nucleus of the trapezoid body may relay input from the ipsilateral ventral cochlear nucleus. These projections offer two routes for indirect, possibly inhibitory input to reach the medial superior olive from both cochlear nuclei. These indirect, inhibitory pathways may parallel the direct excitatory projections the medial superior olive receives from each cochlear nucleus.     

Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei

The projections from the cochlear nucleus to the lateral and medial superior olivary nuclei were studied in the cat by use of retrograde transport of horseradish peroxidase to demonstrate the connections. The medial superior olivary nucleus receives input only from the anterior and posterodorsal subdivisions of the anterior division of the anteroventral cochlear nucleus (AA and APD, respectively; Brawer, Morest, and Kane: J. Comp. Neurol. 155: 251-300, 1974). These two subdivisions are populated almost exclusively by spherical bushy cells. Like the medial superior olivary nucleus, the lateral superior olivary nucleus receives inputs from AA and APD. In addition, the lateral superior olivary nucleus receives projections from the posterior subdivision (AP) of the anterior division and also from the posterior division of the anteroventral cochlear nucleus. The projections to the medial superior olivary nucleus are bilateral, whereas the projections to the lateral superior olivary nucleus are almost entirely ipsilateral. One implication of the results is that the medial superior olivary nucleus receives inputs from only one cell type--the spherical bushy cell--but that, at the least, two cell types project to the lateral superior olivary nucleus. Both the olivary nuclei receive input from most, if not all, of the dorsoventral extent of the anteroventral cochlear nucleus, implying that both receive input from neurons arrayed across the entire frequency representation of the anteroventral cochlear nucleus. All of the projections appear to be organized topographically such that frequency representation is preserved.     

Patterns of reciprocity in auditory thalamocortical and corticothalamic connections: study with horseradish peroxidase and autoradiographic methods in the rat medial geniculate body

The patterns of reciprocity between retrogradely labeled thalamocortical cells of origin and anterogradely projecting corticothalamic axon terminals were studied in the subdivisions of the adult rat medial geniculate body following auditory cortical injections of mixtures of horseradish peroxidase and [3H]leucine. The labeling produced by each method was examined independently, both qualitatively and quantitatively, in adjacent series of tetramethylbenzidine-processed sections and in autoradiographs after 24-96 hour survivals. The distribution and number of labeled cells and axon terminals were assessed separately for each method and compared systematically throughout the rostro-caudal extent of the medial geniculate complex. The principal finding was that zones containing many retrogradely labeled neuronal somata are not completely coextensive with areas of heavy terminal labeling within the medial geniculate body, although there is a gross congruence of thalamocortical-corticothalamic projections. Conversely, we found many zones of autoradiographic silver grains without retrogradely labeled somata in the adjacent sections; in general, the autoradiographic zones of non-reciprocity were more extensive and marked than were retrograde zones of non-reciprocity. The rat medial geniculate complex could be subdivided on the basis of its neuronal organization, cytoarchitecture, fiber architecture, and thalamocortical and corticothalamic connections into three major parts: the ventral, dorsal, and medial divisions. This pattern of organization was comparable, though not identical, to that of the corresponding subdivisions in the cat medial geniculate body (Winer: Adv. Anat. Embryol. Cell Biol. 86:1-98, '85). While the retrograde labeling appeared to mark many of the different types of neurons in each of the three divisions, there were distinct local and quantitative and qualitative differences in the distribution of autoradiographic terminal labeling. The ventral division received the heaviest cortical input, the medial division the least labeling, while the dorsal division was intermediate. Thus, corticogeniculate projections to the ventral division often produced values 20-100 times above background (absolute values: 2,001-10,000 silver grains/14,400 micron2; background: less than 100 silver grains/14,400 micron2); the same projection to the dorsal division usually resulted in grain counts no more than 5-20 times above background (501-2,000/14,400 micron2), while in the medial division the number of silver grains rarely exceeded two to five times the background (201-500/14,400 micron2).(ABSTRACT TRUNCATED AT 400 WORDS)     

The neurons of the medial geniculate body in the mustached bat (Pteronotus parnellii)

The neurons in the medial geniculate body were studied in Golgi preparations from adult mustached bats (Pteronotus parnellii). Their somatic and dendritic configurations were compared with those of cells in other, nonecholocating mammals. A second goal was to use the thalamic nuclear subdivisions derived from Golgi material to integrate the findings in parallel studies of cytoarchitecture, immunocytochemistry, and tectothalamic connections. Three primary divisions are defined. The ventral division is large and has a stereotyped neuronal organization. Medium-sized perikarya (about 10 μm in diameter) represent tufted neurons; the fibrodendritic plexus forms laminae in the lateral part along which midbrain axons terminate. A smaller, possibly intrinsic, neuron with thin, sparse dendrites is rarely impregnated. Neurons in the larger, medial part, which represents frequencies of 60 kHz and higher, have more spherical dendritic fields; their branching pattern remains tufted, and the laminar organization was less evident. The dorsal division is about equal in size, and it has many nuclei and a corresponding neuronal diversity. These neurons are medium-sized except in the suprageniculate nucleus, where many cells are larger. Four dorsal division nuclei are recognized. Each has neurons with radiate or weakly tufted dendritic arbors. Superficial dorsal nucleus neurons are oriented from medial to lateral, imparting a slightly laminated appearance to the neuropil. A few smaller, stellate neurons with modest dendritic domains are present. Suprageniculate nucleus neurons have radiating dendritic fields that project spherically; they have fewer branches than dorsal nucleus neurons. The posterior limitans nucleus is dorsomedial to the suprageniculate nucleus; it has small neurons with long, sparsely branched dendrites. The rostral pole nucleus, included in the dorsal division on cytoarchitectonic grounds, had too few neurons impregnated to reveal its neuronal architecture. The medial division, the smallest of the main parts, is one nucleus with at least six types of cells, including the magnocellular, bushy tufted, disc-shaped, medium-sized multipolar, elongated, and small stellate neurons. There is no laminar arrangement. Many of the neurons resemble those in rodent, marsupial, carnivore, and primate auditory thalamic nuclei. Despite such morphological correspondences, functional differences, such as the evolution of combination sensitivity, suggest that structurally comparable auditory thalamic neurons may subserve diverse physiological representations. © 1994 Wiley-Liss, Inc.     

Intrinsic connections of the rat amygdaloid complex: Projections originating in the central nucleus

Inputs from the amygdaloid and extraamygdaloid areas terminate in various divisions of the central nucleus. To elucidate the interconnections between the different regions of the central nucleus and its connectivity with the other amygdaloid areas, we injected the anterograde tracer, Phaseolus vulgaris-leucoagglutinin (PHA-L) into the capsular, lateral, intermediate, and medial divisions of the central nucleus in rat. There were a number of labeled terminals near the injection site within each division. The intrinsic connections between the various divisions of the central nucleus were organized topographically and originated primarily in the lateral division, which projected to the capsular and medial divisions. Most of the connections were unidirectional, except in the capsular division, which received a light reciprocal projection from its efferent target, the medial division. The intermediate division did not project to any of the other divisions of the central nucleus. Extrinsic projections from the central nucleus to the other amygdaloid nuclei were meager. Light projections were observed in the parvicellular division of the basal nucleus, the anterior cortical nucleus, the amygdalohippocampal area, and the anterior amygdaloid area. No projections to the contralateral amygdala were found. These data show that the central nucleus has a dense network of topographically organized intradivisional and interdivisional connections that may integrate the intraamygdaloid and extraamygdaloid information entering the different regions of the central nucleus. The sparse reciprocal connections to the other amygdaloid nuclei suggest that the central nucleus does not regulate the other amygdaloid regions but, rather, executes the responses evoked by the other amygdaloid nuclei that innervate the central nucleus. J. Comp. Neurol. 395:53–72, 1998. © 1998 Wiley-Liss, Inc.     

Organization of subcortical pathways for sensory projections to the limbic cortex. I. Subcortical projections to the medial limbic cortex in the rat

Subcortical afferent projections to the medial limbic cortex were examined in the rat by the use of retrograde axonal transport of horseradish peroxidase. Small iontophoretic injections of horseradish peroxidase were placed at various locations within the dorsal and ventral cingulate areas, the dorsal agranular and ventral granular divisions of the retrosplenial cortex and the presubiculum. Somata of afferent neurons in the thalamus and basal forebrain were identified by retrograde labeling. Each of the anterior thalamic nuclei was found to project to several limbic cortical areas, although not with equal density. The anterior dorsal nucleus projects primarily to the presubiculum and ventral retrosplenial cortex; the anterior ventral nucleus projects to the retrosplenial cortex and the presubiculum with apparently similar densities; and the anterior medial nucleus projects primarily to the cingulate areas. The projections from the lateral dorsal nucleus to these limbic cortical areas are organized in a loose topographic fashion. The projection to the presubiculum originates in the most dorsal portion of the lateral dorsal nucleus. The projection to the ventral retrosplenial cortex originates in rostral and medial portions of the nucleus, whereas afferents to the dorsal retrosplenial cortex originate in caudal portions of the lateral dorsal nucleus. The projection to the cingulate originates in the ventral portion of the lateral dorsal nucleus. Other projections from the thalamus originate in the intralaminar and midline nuclei, including the central lateral, central dorsal, central medial, paracentral, reuniens, and paraventricular nuclei, and the ventral medial and ventral anterior nuclei. In addition, projections to the medial limbic cortex from the basal forebrain originate in cells of the nucleus of the diagonal band. Projections to the presubiculum also originate in the medial septum. These results are discussed in regard to convergence of sensory and nonsensory information projecting to the limbic cortex and the types of visual and other sensory information that may be relayed to the limbic cortex by these projections.     

Direct synaptic connections of axons from superior colliculus with identified thalamo-amygdaloid projection neurons in the rat: Possible substrates of a subcortical visual pathway to the amygdala

The aim of the present study was to identify synaptic contacts from axons originating in the superior colliculus with thalamic neurons projecting to the lateral nucleus of the amygdala. Axons from the superior colliculus were traced with the anterograde tracers Phaseolus vulgaris leucoagglutinin or the biotinylated and fluorescent dextran amine “Miniruby.” Thalamo-amygdaloid projection neurons were identified with the retrograde tracer Fluoro-Gold. Injections of Fluoro-Gold into the lateral nucleus of the amygdala labeled neurons in nuclei of the posterior thalamus which surround the medial geniculate body, viz. the suprageniculate nucleus, the medial division of the medial geniculate body, the posterior intralaminar nucleus, and the peripeduncular nucleus. Anterogradely labeled axons from the superior colliculus terminated in the same regions of the thalamus. Tecto-thalamic axons originating from superficial collicular layers were found predominantly in the suprageniculate nucleus, whereas axons from deep collicular layers were detected in equal density in all thalamic nuclei surrounding the medial geniculate body. Double-labeling experiments revealed an overlap of projection areas in the above-mentioned thalamic nuclei. Electron microscopy of areas of overlap confirmed synaptic contacts of anterogradely labeled presynaptic profiles originating in the superficial layers of the superior colliculus with retrogradely labeled postsynaptic profiles of thalamo-amygdaloid projection neurons. These connections may represent a subcortical pathway for visual information transfer to the amygdala. J. Comp. Neurol. 403:158–170, 1999. © 1999 Wiley-Liss, Inc.