Thalamic connections with limbic cortex. II. Corticothalamic projections

The corticothalamic projections from the cat limbic cortex have been investigated with anterograde and retrograde axonal transport techniques. Five limbic cortical areas—the anterior limbic area, the cingular area, the granular and dysgranular retrosplenial areas, and the presubiculum—were identified on the basis of their cytoarchitecture. Emphasis was placed on determining the laminar distribution of the cells of origin of the efferent projections, the projection pathways, and the sites of termination within the thalamus. Projections to the thalamus originate in layers V and VI of limbic cortex. In the cingular region the cells of origin are predominantly in layer V and to a lesser extent in layer VI, while the majority of cells projecting from the more caudal retrosplenial areas and presubiculum are in layer VI. There are two fiber pathways from each cortical area to the thalamus. One system of fibers passes through the internal capsule and lateral thalamic peduncle, and a second system travels in the cingulate fasciculus before piercing the corpus callosum to join the postcommissural fornix. The lateral dorsal nucleus and the anterior nuclear group, including the anterior dorsal, anterior ventral, and anterior medial nuclei, are the major thalamic recipients of projections from limbic cortex. Corticothalamic projections also terminate sparsely in the midline and intralaminar nuclear complex, including the central lateral, central dorsal, paracentral, central medial, rhomboid, and reuniens nuclei. Projections from the anterior limbic area project predominantly to the anterior medial, centrall lateral, and paracentral nuclei. The anterior ventral nucleus, anterior medial nucleus, and lateral dorsal nucleus are the major thalamic recipients of projections from the cingular area, the granular and dysgranular retro-splenial areas, and the presubiculum. It appears that the anterior dorsal nucleus receives afferents only from the dysgranular retrosplenial area. Bilateral corticothalamic projections were found in the anterior medial, dorsal medial, central lateral, central medial, paracentral, and reuniens nuclei.     

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.     

Thalamic connections with limbic cortex. I. Thalamocortical projections

The thalamocortical projections to limbic cortex in the cat have been studied with retrograde and anterograde axonal transport techniques. Five limbic cortical areas were identified on the basis of cytoarchitecture. The five areas are the anterior limbic area, the cingular area, the dorsal and ventral retrosplenial areas, and the presubiculum. Each of these cortical areas received small injections of horseradish peroxidase, and the afferent thalamic nuclei were identified by retrograde labelling of cells. The cortical projection of each of the anterior thalamic nuclei and the lateral dorsal nucleus was determined autoradiographically. Each of the anterior thalamic nuclei and the lateral dorsal nucleus projects to limbic cortex by two pathways. One group of fibers leaves the rostral thalamus by the fornix, pierces the corpus callosum, and joins the cingulate fasciculus to reach limbic cortex. The other group travels through the lateral thalamic peduncle and internal capsule. The anterior ventral nucleus projects primarily to the dorsal retroslenial area, particularly to layer I, the deep portion of layer II, and superficial portion of layer III. Sparse projections also exist to the ventral retrosplenial area, the cingular area, and the presubiculum. Very sparse projections to the anterior limbic area are seen. The anterior dorsal nucleus projects primarily to the ventral retrosplenial area, particularly layers I, the deep portion of layer II, and superficial layer III. Sparse projections exist to the dorsal retrosplenial area and presubiculum, but apparently no projections exist to the cingular or anterior limbic area. The anterior medial nucleus projects primarily to layers I and superficial III of the ventral retrosplenial area. Sparse projections exist to each of the other limbic cortical areas. The lateral dorsal nucleus projects extensively onto limbic cortex. Prominent projections occur to layer I, the external granular layer and lamina dessicans of the presubiculum, layers I and III-IV of the dorsal retrosplenial area, and layers I, III, and IV of the cingular area. Sparse projections occur to the ventral retrosplenial area and the anterior limbic areas. Thalamocortical projections also originate in the midline and intralaminar nuclei including the central medial reuniens, rhomboid, paracentral, central lateral, and central dorsal nuclei. These data indicate that the anterior thalamic nuclei project upon limbic cortex in a complex manner. Further, the projections to limbic cortex from the anterior nuclei overlap with projections from the lateral dorsal nucleus. This overlap of thalamic projections onto limbic cortex suggests a convergence of information from nonprimary sensory systems with information from the classical limbic system.     

Cholinergic innervation of the human thalamus: dual origin and differential nuclear distribution.

The cholinergic innervation of the human thalamus was studied with antibodies against the enzyme choline acetyltransferase (ChAT) and nerve growth factor receptor (NGFr). Acetylcholinesterase histochemistry was used to delineate nuclear boundaries. All thalamic nuclei displayed ChAT-positive axons and varicosities. Only the medial habenula contained ChAT-positive perikarya. Some intralaminar nuclei (central medial, central lateral, and paracentral), the reticular nucleus, midline nuclei (paraventricular and reuniens), some nuclei associated with the limbic system (anterodorsal nucleus and medially situated patches in the mediodorsal nucleus) and the lateral geniculate nucleus displayed the highest density of ChAT-positive axonal varicosities. The remaining sensory relay nuclei and the nuclei interconnected with the motor and association cortex displayed a lower level of innervation. Immunoreactivity for NGFr was observed in cholinergic neurons of the basal forebrain but not in cholinergic neurons of the upper brainstem. The contribution of basal forebrain afferents to the cholinergic innervation of the human thalamus was therefore studied with the aid of NGFr-immunoreactive axonal staining. The anterior intralaminar nuclei, the reticular nucleus, and medially situated patches in the mediodorsal nucleus displayed a substantial number of NGFr-positive varicose axons, presumably originating in the basal forebrain. Rare NGFr-positive axonal profiles were also seen in many of the other thalamic nuclei. These observations suggest that thalamic nuclei affiliated with limbic structures and with the ascending reticular activating system are likely to be under particularly intense cholinergic influence. While the vast majority of thalamic cholinergic input seems to come from the upper brainstem, the intralaminar and reticular nuclei, and especially medially situated patches within the mediodorsal nucleus also appear to receive substantial cholinergic innervation from the basal forebrain.     

Afferent fibers to rat cingulate cortex

Afferent fibers to the rat cingulate cortex were studied by the retrograde labeling technique using horseradish peroxidase-wheat germ agglutinin conjugate as the tracer. The results showed that the posterior cingulate cortex, but not the anterior, received input from the anterior dorsal and anterior ventral nuclei of the anterior thalamic group of nuclei (part of the so-called limbic thalamus), and from the subicular complex. The anterior cingulate cortex, but not the posterior, received input from the mediodorsal and ventral thalamic nuclei. Both posterior and anterior cingulate cortex received input from the hippocampus pars anterior; claustrum; globus pallidus; nucleus of the diagonal band of Broca (a particularly reliable source of afferent fibers); anterior medial, lateral, rhomboid, and reuniens nuclei of the thalamus; region of the medial forebrain bundle; periventricular nucleus of the hypothalamus; the dorsal and median raphe; and the locus ceruleus. Corticocortical projections were seen anterior, posterior, and lateral to the injection site, and in the homologous contralateral cingulate cortex. The results demonstrate a prominent source of cingulate afferent fibers from the subicular complex, provide evidence for a functional division of anterior and posterior cingulate cortices in the rat, and provide information about the relative anatomic importance of cingulate afferent fibers from those different regions.     

Anterior thalamic afferents from the mamillary body and the limbic cortex in the rat

Anterior thalamic afferents from the mamillary body and the limbic cortex were studied by using single and double retrograde transport methods in the rat. The medial mamillary nucleus was divided on the basis of the cytoarchitecture into four subnuclei: the pars medialis centralis, pars medialis dorsalis, pars lateralis, and pars basalis. Extensive connections were seen between each of these subdivisions of the mamillary body and the anterior thalamic nuclei, topographically organized so that the anteromedial thalamic nucleus receives projections exclusively from the pars medialis centralis, while the anteroventral thalamic nucleus receives projections from the pars medialis dorsalis and pars lateralis. Nuclei in the dorsal half of these two mamillary subdivisions project predominantly to the medial half of the anteroventral thalamic nucleus, and those in the ventral half to the lateral half of the nucleus. The pars basalis was found to have numerous projections to the magnocellular part of the anteroventral nucleus. All limbic cortical areas send projections bilaterally to all regions of the anteromedial nucleus as well as to the parvicellular parts of the anteroventral thalamic nucleus, while the anterodorsal nucleus receives ipsilateral projections originating exclusively from the preagranular, anterior limbic, and cingular regions. The magnocellular part of the anteroventral nucleus, however, receives only ipsilateral projections from all of the limbic cortex. Some neurons in the infralimbic region also project bilaterally to all of the anterior thalamic nuclei except the anterodorsal nucleus. All of these cortical projections to the anterior thalamus originate in layers V and VI of the limbic cortex.     

Functional heterogeneity of the limbic thalamus: From hippocampal to cortical functions

Today, the idea that the integrity of the limbic thalamus is necessary for normal memory functions is well established. However, if the study of thalamic patients emphasized the anterior and the mediodorsal thalamus as the critical thalamic loci supporting cognitive functions, clinical studies have so far failed to attribute a specific role to each of these regions. In view of these difficulties, we review here the experimental data conducted in rodents harboring specific lesions of each thalamic region. These data clearly indicate a major functional dissociation within the limbic thalamus. The anterior thalamus provides critical support for hippocampal functions due to its cardinal location in the Papez circuit, while the mediodorsal thalamus may signal relevant information in a circuit encompassing the basolateral amygdala and the prefrontal cortex. Interestingly, while clinical studies have suggested that diencephalic pathologies may disconnect the medial temporal lobe from the cortex, experimental studies conducted in rodent show how this may differently affect distinct temporo-thalamo-cortical circuits, sharing the same general organization but supporting dissociable functions.     

Collateral innervation of the medial and lateral prefrontal cortex by amygdaloid, thalamic, and brain-stem neurons

The distribution of the afferents to the rat's prefrontal cortex originating in the thalamic mediodorsal nucleus and the amygdala was investigated with two fluorescent tracers. Special emphasis was laid on detecting the loci of neurons which project via axonal collaterals into both lateral and medial portions of the prefrontal cortex. It was found that a high number of neurons of the anterior portion of the basolateral amygdaloid nucleus terminate via collaterals in both the medial and lateral subfields of the prefrontal cortex. On the other hand, only a small number of mediodorsal thalamic cells were found to project to both sides of the prefrontal hemisphere via bifurcating axonal collaterals. These cells were situated exclusively in the lateral part of the medial segment of the mediodorsal nucleus. The majority of both thalamic and amygdaloid neurons with bifurcating axons originate from subregions whose cells innervate primarily the medial prefrontal cortex. In brain-stem, neurons of the nucleus raphé dorsalis also project via collaterals to the medial and lateral prefrontal regions. Furthermore, neurons of the dorsal and ventral premamillary nuclei, the lateral mamillary nucleus, the ventral tegmental area of Tsai, and the ventral tegmental nucleus of Gudden were found to project to the medial prefrontal cortex. Our results indicate a differential collateral organization of thalamic and amygdaloid afferents to prefrontal cortical fields. The anterior basolateral amygdala (which innervates via collaterals both the medial and lateral prefrontal subfields) may add a common input to either subfield, such as information on the significance of incoming stimuli to the animal's behavior, while the mediodorsal nucleus (whose segments are principally connected to only one prefrontal subfield) may add segment-specific information, for example, of a spatial-cognitive nature for the lateral segment and of an emotional nature for the central and medial segments. The existence of a basolateral limbic circuit, composed of the amygdala, the thalamic mediodorsal nucleus, and the prefrontal cortex, is confirmed and knowledge on its interconnectivity is extended. From an anatomical point of view these data provide arguments for both unitary and diverging functions of the prefrontal cortex.     

Topographical organization of the thalamic afferent connections to the motor cortex in the cat

The topographical distribution of the cortical afferent connections to the different subdivisions of the motor cortex (MC) was studied in adult cats. The retrograde axonal transport of horseradish peroxidase technique was used. Small single injections of the enzyme were made in the entire MC, including the hidden regions in the depth of the sulcus cruciatus. The areal location and density of the subsequent thalamic neuronal labeling were evaluated in each case. Comparison of the results obtained in the various cases shows that the following: (1) The ventral anterior-ventral lateral complex is the principal thalamic source of afferents to the MC. (2) The ventral medial, dorsal medial, the different components of the posterior thalamic group (lateral, medial, and ventral posteroinferior and suprageniculate nuclei), and the intralaminar, lateral anterior, lateral intermediate, lateral medial, and anteromedial thalamic nuclei are also thalamic sites in which neural projections to the MC arise. (3) The thalamocortical projections to the MC are sequentially organized. The connections arising from the lateral part of the thalamus end in the region of area 4 that is situated medially in the superior lip of the sulcus cruciatus and in the posterior sigmoid gyrus. The projections originating in the most medial thalamic regions terminate in that region of area 6a beta which is located in the medial part of the inferior lip of the cruciate sulcus, and in the anterior sigmoid gyrus. Moreover, the ventral thalamic areas send connections to the most anteriorly located zones of the MC, while the most dorsal thalamic ones project to the most posteriorly located parts of the MC. (4) This shift in the thalamocortical connections is not restrained by cytoarchitectonic boundaries, either in the thalamus or in the cortex. (5) The populations of thalamocortical cells which project to neighboring MC subdivisions exhibit consistent overlapping among themselves. (6) These findings suggest, moreover, that the basal ganglia and the cerebellar projections to the MC through the thalamus are arranged in a number of parallel pathways, which may occasionally overlap.     

'Non-specific' cholinesterase-containing neurons of the dorsal thalamus project to medial limbic cortex

Thalamocortical neurons that contain 'non-specific' cholinesterase (ChE) were studied with cholinesterase histochemistry and experimental axonal tracing techniques in adult rats. In addition to the presence of ChE that is ubiquitous in capillary endothelium, neurons that contain ChE are found in 3 distinct regions of the dorsal thalamus, the thalamic reuniens nucleus (Re), the anterior dorsal nucleus (AD) and a region that includes the lateral part of the central lateral nucleus (CL) and the ventral portion of the lateral dorsal nucleus (LD). ChE activity appears light in cerebral cortex in general but histochemical staining is slightly greater in neuropil of the cingulate gyrus. Anterograde transport techniques with autoradiography demonstrated that neurons in the LD-CL region project to anterior cingulate cortex and the dorsal retrosplenial area. Anterograde degeneration techniques demonstrated that AD projects primarily to ventral retrosplenial cortex. Injections of horseradish peroxidase (HRP) in the anterior cingulate cortex resulted in double labeled cells (cells containing both ChE and HRP reaction products) primarily in LD and CL. HRP injections into ventral retrosplenial cortex resulted in double labeled cells in AD and Re. HRP injections in the subiculum resulted in double labeled cells in Re. Lesions placed in the region of thalamocortical projections resulted in a loss of ChE in the ipsilateral cingulate gyrus, as measured both histochemically and enzymatically. The finding that neurons containing ChE project to medial limbic cortex suggests that the ChE may be involved in the function of the thalamocortical component of the limbic system.     

Visceral cortex: integration of the mucosal senses with limbic information in the rat agranular insular cortex

The organization of the subcortical and cortical connections of the rat agranular insular cortex was examined. Retrogradely transported dyes were used to map the agranular insular cortex efferents to brainstem visceral nuclei (the nucleus of the solitary tract and the parabrachial nucleus), to gustatory-visceral and limbic thalamic nuclei (medial ventrobasal and mediodorsal thalamus, respectively), and to association cortex (medial prefrontal and contralateral agranular insular cortex). The results revealed that a specific area within the ipsilateral agranular insular cortex projected to all of the subcortical and cortical areas listed above. This area of overlap in the agranular insular cortex stretched from the level of the genu of the corpus callosum rostrally to the crossing of the anterior commissure caudally. Anterograde projections from the medial ventrobasal and mediodorsal thalamus and from the olfactory bulb to the agranular insular cortex were mapped with wheat germ agglutinin conjugated to horseradish peroxidase. The terminal cortical projections from these areas were generally separate, except in an area where they overlap immediately medial to the rhinal fissure in the agranular insular cortex. This overlap area matched the area in the agranular insular cortex where there was an overlap of cortical efferent cells projecting to the brainstem, thalamus, and association cortex, as revealed in the retrograde tracing studies. We refer to this region of convergence in the agranular insular cortex as the visceral cortex, and suggest its involvement in the efficient integration of specific visceral sensory stimuli with correlated limbic or motivational consequences. The visceral cortex may help regulate the organism's visceral response to stress.     

Stress induces Fos expression in neurons of the thalamic paraventricular nucleus that innervate limbic forebrain sites

The paraventricular nucleus of the thalamus (PVT) is a midline thalamic nucleus that responds strongly to exposure to various stressors. Many of the projection targets of PVT neurons, including the medial prefrontal cortex, nucleus accumbens, and central/basolateral nuclei of the amygdala, are also activated by stress. We sought to determine if PVT neurons that respond to stress are those that project to one or more of these forebrain sites. Retrograde tract tracing combined with immunohistochemical detection of Fos protein-like immunoreactivity was used to assess the activation of target-specific populations of PVT projection neurons by mild footshock stress in the rat. Stress markedly increased Fos protein-like immunoreactivity in PVT neurons, but without regard to the projection target of the thalamic neurons. Thus, the percentage of PVT cells that were retrogradely labeled from either the prefrontal cortex, nucleus accumbens, or amygdala, and that expressed Fos-like immunoreactivity did not differ substantially across the three forebrain sites. These data suggest that the PVT may have a role as a generalized relay for information relating to stress, and may serve an important role in the stress-induced activation of limbic forebrain areas.     

Organization of thalamic projections in the nucleus accumbens and the caudate nucleus in cats and its relation with hippocampal and other subcortical afferents

The organization of thalamic projections in the nucleus accumbens (NA) and the caudate nucleus of cats and its relation to other subcortical striatal afferents were studied with a retrograde tracing technique by use of lectin-conjugated horseradish peroxidase. The study showed that the paraventricular and medial parafascicular nuclei (PF) of the thalamus project to the medial NA and the parataenial and medial PF project to the lateral NA. The ventral tegmental area and substantia nigra pars dorsalis (SNpd) project to medial and lateral NA. The midline thalamic nuclei, rostral intralaminar nuclei, ventroanterior nucleus, medial and lateral PF, lateral posterior complex, and nucleus limitans project to medial caudate nucleus. The most medial substantia nigra pars compacta (SNpc) and rostral SNpd project to medial caudate nucleus. The center median, ventrolateral, and the central lateral nuclei of thalamus, SNpc, and SNpd project to lateral caudate nucleus. These results suggest that the thalamic and subcortical nuclei known to connect with the limbic and frontal cortices project to NA and medial caudate nucleus. Those thalamic nuclei connected with the motor system project to lateral caudate nucleus. The hippocampus projects selectively to medial NA. The amygdala, raphe, and other mesencephalic nuclei project only to NA and medial caudate nucleus. The organization of hippocampal, amygdala, and other subcortical afferents suggests that NA and caudate nucleus can be separated into medial "limbic" and lateral nonlimbic "sensory-motor" compartments. A brief review of the distribution pattern of some neurotransmitters, neuropeptides, and their receptors and behavior studies provides additional support to the concept that the striatum can be divided into several subcompartments.     

The Pathological Substrate of Limbic Epilepsy: Neuronal Loss in the Medial Dorsal Thalamic Nucleus as the Consistent Change

Summary: Purpose : The focus of research in limbic epilepsy has been the hippocampus because of its well-known pathology of hippocampal atrophy and sclerosis as well as the strong propensity for this structure to seize under a variety of circumstances. There is ample evidence, however, for pathological alterations in other regions of the limbic system in limbic/mesial temporal lobe epilepsy, including the amygdala, the entorhinal cortex, and, in some cases, the thalamus. In this preliminary evaluation of the pathological substrate for limbic epilepsy, we wished to determine if there was consistent anatomic change at extrahippocampal sites.
Methods : We compared paraffin sections of brains from rats with chronic spontaneous limbic epilepsy and age-matched controls to determine the consistency of the pathology at five sites: the hippocampus, amygdala, entorhinal cortex, piriform cortex, and medial dorsal thalamus.
Results : In a qualitative evaluation of these sections taken from standardized positions, we found that the medial dorsal thalamic nucleus in the epileptic animals was the site that was consistently involved with neuronal loss. With all other sites, at least several animals had qualitatively normal tissue.
Conclusions : This finding suggests that neuronal loss in the medial dorsal thalamus may be the consistent pathology in limbic epilepsy, at least in an animal model of the disorder. The presence of a structurally abnormal subcortical region with broad connections to the limbic sites involved with chronic epilepsy may have implications for our understanding of the pathophysiology of this disorder.     

Connections between cells of the internal capsule,thalamus, and cerebral cortex in embryonic rat

The aim of our study is to understand the development of the earliest connections in the mammalian pallium by documenting the distribution of cells and fibres labelled from the dorsal and ventral thalamus, internal capsule, perirhinal, and dorsal cortex during the period between embryonic day (E) 14 and 17 by using carbocyanine dye tracing in fixed embryonic rat brains. Dye placed in the thalamus of E14 brains backlabels cells in the thalamic reticular nucleus and within the primitive internal capsule. Both anterograde and retrograde tracing confirmed that the first corticofugal projections reach the internal capsule by E14. At E15–E16, after the first cortical plate cells have migrated into the lateral cortex, some cells of the cortical plate and subplate and marginal zone, are backlabelled from the internal capsule, but still not from the dorsal thalamus, even with very long incubation periods. Crystal placement into the perirhinal cortex at E14–E15 labels numerous cells within the internal capsule, whereas no such cells are revealed from dorsal cerebral cortex until E17, suggesting that internal capsule cells establish early connections with the perirhinal and ventral but not dorsal cortex. We propose that the growth of axons from cortex to dorsal thalamus is delayed in two regions: first from E14–E15 at the lateral entrance of the internal capsule and then, from E16, closer to the thalamus, probably within the thalamic reticular nucleus. Subplate projections reach the proximity of the diencephalon at an early stage, but they might never enter the dorsal thalamus. J. Comp. Neurol. 413:1–25, 1999. © 1999 Wiley-Liss, Inc.     

Collateral projections of single neurons in the posterior thalamic region to both the temporal cortex and the amygdala: a fluorescent retrograde double-labeling study in the rat

It has been reported that the acoustic thalamus of the rat sends projection fibers to both the temporal cortical areas and the lateral amygdaloid nucleus to mediate conditioned emotional responses to an acoustic stimulus. In the present study, fluorescent retrograde double labeling with Fast Blue and Diamidino Yellow has been used in the rat to examine whether single neurons in the posterior thalamic region send axon collaterals to both the temporal cortical areas and lateral amygdaloid nucleus. One of the tracers was injected into the lateral amygdaloid nucleus and the other into the temporal cortical areas close to the rhinal sulcus. Neurons double-labeled with both tracers were found mainly in the posterior intralaminar nucleus and suprageniculate nucleus, and to a lesser extent in the subparafascicular nucleus and medial division of the medial geniculate nucleus. No double-labeled neurons were seen in either the dorsal or ventral division of the medial geniculate nucleus. When one of the tracers was injected into the lateral amygdaloid nucleus and the other into either the dorsal portion of the temporal cortex, the dorsal portion of the entorhinal cortex, or the posterior agranular insular cortex, no double-labeled neurons were found in the posterior thalamic region. The present results indicate that a substantial number of single neurons in the acoustic thalamus project to both the limbic cortical areas and lateral amygdaloid nucleus by way of axon collaterals. These neurons may be implicated in affective and autonomic components of responses to multi-sensory stimuli, including acoustic ones. J. Comp. Neurol. 384:59-70, 1997. © 1997 Wiley-Liss, Inc.     

Thalamic Input to Representations of the Teeth,Tongue, and Face in Somatosensory Area 3b of Macaque Monkeys

Representations of the parts of the oral cavity and face in somatosensory area 3b of macaque monkeys were identified with microelectrode recordings and injected with different neuroanatomical tracers to reveal patterns of thalamic projections to tongue, teeth, and other representations in primary somatosensory cortex. The locations of injection sites and resulting labeled neurons were further determined by relating sections processed to reveal tracers to those processed for myeloarchitecture in the cortex and multiple architectural stains in the thalamus. The ventroposterior medial subnucleus (VPM) for touch was identified as separate from the ventroposterior medial parvicellular nucleus (VPMpc) for taste by differential expression of several types of proteins. Our results revealed somatotopically matched projections from VPM to the part of 3b representing intra‐oral structures and the face. Retrogradely labeled cells resulting from injections in area 3b were also found in other thalamic nuclei including: anterior pulvinar (Pa), ventroposterior inferior (VPI), ventroposterior superior (VPS), ventroposterior lateral (VPL), ventral lateral (VL), center median (CM), central lateral (CL), and medial dorsal (MD). None of our injections, including those into the representation of the tongue, labeled neurons in VPMpc, the thalamic taste nucleus. Thus, area 3b does not appear to be involved in processing taste information from the thalamus. This result stands in contrast to those reported for New World monkeys. J. Comp. Neurol. 521:3954–3971, 2013. © 2013 Wiley Periodicals, Inc.     

Parallel but separate inputs from limbic cortices to the mammillary bodies and anterior thalamic nuclei in the rat

The proposal that separate populations of subicular cells provide the direct hippocampal projections to the mammillary bodies and anterior thalamic nuclei was tested by placing two different fluorescent tracers in these two sites. In spite of varying the injection locations within the mammillary bodies and within the three principal anterior thalamic nuclei and the lateral dorsal thalamic nucleus, the overall pattern of results remained consistent. Neurons projecting to the thalamus were localized to the deepest cell populations within the subiculum while neurons projecting to the mammillary bodies consisted of more superficially placed pyramidal cells within the subiculum. Even when these two cell populations become more intermingled, e.g., in parts of the intermediate subiculum, almost no individual cells were found to project to both diencephalic targets. In adjacent limbic areas, i.e., the retrosplenial cortex, postsubiculum, and entorhinal cortex, populations of cells that project to the anterior thalamic nuclei and mammillary bodies were completely segregated. This segregated pattern included afferents to those nuclei comprising the head‐direction system. The sole exception was a handful of double‐labeled cells, mainly confined to the ventral subiculum, that were only found after pairs of injections in the anteromedial thalamic nucleus and mammillary bodies. The projections to the anterior thalamic nuclei also had a septal‐temporal gradient with relatively fewer cells projecting from the ventral (temporal) subiculum. These limbic projections to the mammillary bodies and anterior thalamus comprise a circuit that is vital for memory, within which the two major components could convey parallel, independent information. J. Comp. Neurol. 518:2334–2354, 2010. © 2010 Wiley‐Liss, Inc.     

Prosencephalic afferents to the mediodorsal thalamic nucleus

The afferent projections from the prosencephalon to the mediodorsal thalamic nucleus (MD) were studied in the cat by use of the method of retrograde transport of horseradish peroxidase (HRP). Cortical and subcortical prosencephalic structures project bilaterally to the MD. The cortical afferents originate mainly in the ipsilateral prefrontal cortex. The premotor, prelimbic, anterior limbic, and insular agranular cortical areas are also origins of consistent projections to the MD. The motor cortex, insular granular area, and some other cortical association areas may be the source of cortical connections to the MD. The subcortical projections originate principally in the ipsilateral rostral part of the reticular thalamic nucleus and the rostral lateral hypothalamic area. Other parts of the hypothalamus, the most caudal parts of the thalamic reticular nucleus, the basal prosencephalic structures, the zona incerta, the claustrum, and the entopeduncular and subthalamic nuclei are also sources of projections to the MD. Distinct, but somewhat overlapping areas of the prosencephalon project to the three vertical subdivisions of MD (medial, intermediate, and lateral). The medial band of the MD receives a small number of prosencephalic projections; these arise mainly in the caudal and ventral parts of the prefrontal cortex. Cortical projections also arise in the infralimbic area, while subcortical projections originate in the medial part of the rostral reticular thalamic nucleus and lateral hypothalamic area. The intermediate band of the MD receives the largest number of fibers from the prosencephalon. These arise principally in the intermediate and dorsal part of the lateral and medial surface of the prefrontal cortex, the premotor cortex, and the prelimbic and agranular insular areas. Projections also originate in basal prosencephalic formations (preoptic area, Broca's diagonal band, substantia innominata, and olfactory tubercle), rostral reticular thalamic nucleus, and lateral hypothalamic area. A large number of prosencephalic structures also project to the lateral band of the MD. These are mainly the most dorsal and caudal parts of the lateral and medial surface of the prefrontal cortex, the premotor and motor cortices, and the prelimbic, anterior limbic, and insular areas. Projections arise also in the lateral rostral and caudal parts of the reticular thalamic nucleus, the zona incerta, the lateral and dorsal hypothalamic areas, the claustrum, and the entopeduncular nucleus. These and previous results demonstrate a gradation in the afferent connections to the three subdivisions of the MD. Brain structures related to the olfactory sensory modality and with allocortical formations of the limbic system project principally to the medial band of the MD. The intermediate band of the MD receives subcortical and cortical projections from structures mainly related to the limbic system and cortical regions related to sensory association cortices. The lateral band of the MD receives projections mainly originating in structures related to complex sensory associative processes and to the motor system (especially from brainstem and cortical structures implicated in the regulation of eye movements).