Projection from the nucleus reuniens thalami to the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris-leucoagglutinin

In order to study the morphological substrate of possible thalamic influence on the cells of origin and area of termination of the projection from the entorhinal cortex to the hippocampal formation, we examined the pathways, terminal distribution, and ultrastructure of the innervation of the hippocampal formation and parahippocampal region by the nucleus reuniens of the thalamus (NRT). We employed anterograde tracing with Phaseolus vulgaris-leucoagglutinin (PHA-L). Injections of PHA-L in the NRT produce fiber and terminal labeling in the stratum lacunosum-moleculare of field CA1 of the hippocampus, the molecular layer of the subiculum, layers I and III/IV of the dorsal subdivision of the lateral entorhinal area (DLEA), and layers I and III-VI of the ventral lateral (VLEA) and medial (MEA) divisions of the entorhinal cortex. Terminal labeling is most dense in the stratum lacunosum-moleculare of field CA1, the molecular layer of the ventral part of the subiculum, MEA, and layer I of the perirhinal cortex. In layer I of the caudal part of DLEA and in MEA, terminal labeling is present in clusters. Injections in the rostral half of the NRT produce the same distribution in the hippocampal region as those in the caudal half of the NRT, although the projections from the rostral half of the NRT are much stronger. A topographical organization is present in the projections from the head of the NRT, so that the dorsal part projects predominantly to dorsal parts of field CA1 and the subiculum and to lateral parts of the entorhinal cortex, whereas the ventral part projects in greatest volume to ventral parts of field CA1 and the subiculum and to medial parts of the entorhinal cortex. The distribution of the reuniens fibers coursing in the cingulate bundle was determined by comparing cases with and without transections of this bundle. The fibers carried by the cingulate bundle exclusively innervate field CA1 of the hippocampus, the dorsal part of the subiculum, and the presubiculum and parasubiculum. They participate in the innervation of the ventral part of the subiculum and MEA. Electron microscopy was used to visualize the axon terminals of PHA-L-labeled reuniens fibers. These terminals possess spherical synaptic vesicles and form asymmetric synaptic contacts with dendritic spines or with thin shafts of spinous dendrites.(ABSTRACT TRUNCATED AT 400 WORDS)     

Heterotopic Cortical Afferents to the Medial Prefrontal Cortex in the Rat. A Combined Retrograde and Anterograde Tracer Study

Cortical afferent projections towards the medial prefrontal cortex (mPFC) were investigated with retrograde and anterograde tracer techniques. Heterotopical afferent projections to the medial prefrontal cortex arise in secondary, or higher order, sensory areas, motor areas and paralimbic cortices. On the basis of these projections three subfields can be discriminated within the mPFC. (1) The ventromedial part of mPFC, comprising the pre- and infralimbic areas, receives mainly projections from the perirhinal cortex. (2) The caudal two-thirds of the dorsomedial PFC, comprising frontal area 2 and the dorsal anterior cingulate area, receives projections from the secondary visual areas, the posterior agranular insular area and the retrosplenial areas. (3) The rostral one-third of the dorsomedial PFC is the main recipient of projections from the somatosensory and motor areas and the posterior agranular insular area. The laminar distribution of cells projecting to the mPFC varies considerably in the different cortical areas, just as the laminar distribution of termination of their fibres within the mPFC does. It is concluded that the corticocortical connections corroborate with subcortical connectivity in attributing to the mediodorsal projection cortex of the rat functions which are comparable to those of certain prefrontal, premotor and anterior cingulate areas in the monkey.     

Efferent projections from limbic cortex of the temporal pole to the magnocellular medial dorsal nucleus in the rhesus monkey

The efferent projection from the rostral cortices of the temporal lobe to the magnocellular division of the medial dorsal nucleus (MDmc) was studied in the rhesus monkey (Macaca mulatta). The temporal pole region contains four architectonically defined cortical divisions. Medially, the allocortex of the temporal limb of the pyriform cortex is annexed to the temporal lobe neocortices at the limen insulae. Two transitional neocortices, the periallocortical and proisocortical divisions, are situated subjacent to the pyriform area. They make up the largest part of the temporal tip and separate the pyriform cortex from the architecturally more progressive isocortical divisions of the pole found laterally at the rostral ends of the superior and inferior temporal gyri. Neuroanatomical tracers were injected into each of the major divisions of the temporal pole cortex, and the injection site locations were characterized cytoarchitectonically as well as geographically. Injections of tritiated amino acids into pyriform allocortex or into the transitional neocortical fields revealed an efferent projection to the magnocellular medial dorsal nucleus. The terminal field was characterized by a mosaic type of organization and contained discrete zones of axonal termination in which bursts of coarse label surrounded neuronal perikarya and their proximal dendrites. A similar projection was also observed when horseradish peroxidase was injected into the transitional cortices. However, perikarya participating in the terminal clusters were not retrogradely labeled. Intracortical injections restricted to lateral polar isocortex did not result in either anterograde or retrograde transport of label to MDmc. These findings demonstrate a nonreciprocal, corticofugal pathway to MDmc that originates in the phylogenetically older districts of the temporal pole. The conduction of limbic sensory information directly from temporal neocortex to the medial thalamus may play a fundamental role in human and primate memory.     

An analysis of the efferent connections of the septal area in the cat

The neuroanatomical organization of the efferent connections of the septal area in the cat was analyzed by the use of anterograde ([3H]leucine radioautography) and retrograde (horseradish peroxidase histochemistry) tracing techniques. The results indicate that the lateral septal nucleus projects to the nuclei of the diagonal band, preoptic area, lateral hypothalamus, and supramammillary region. The projections of the septofimbrial nucleus supply the nuclei of the diagonal band and the medial habenular nucleus. Projection targets of the vertical limb of the diagonal band are widespread and include the preoptic area, lateral hypothalamus, anterior limbic cortex, amygdala, medial habenular nucleus, interpeduncular nucleus and hippocampal formation. The projection from the vertical limb to the hippocampal formation is organized in a topographical manner in such a fashion that cells positioned near the midline project to the dorsal hippocampus and adjoining subicular cortex while fibers originating from cells situated more laterally project to more ventral parts of the hippocampal formation. In general, the projections from the horizontal limb were similar to those from the vertical limb, but several differences were noted. Fibers arising from the horizontal limb are distributed to the ventral tegmental area and interpeduncular nucleus but this region seems to lack a projection to either the habenular complex or to the ventral aspect of the hippocampal formation. Fibers arising from the bed nucleus of the anterior commissure are distributed to the preoptic region, lateral hypothalamus, supramammillary region, posterior aspect of the medial mammillary nucleus and lateral habenular nucleus.     

Bihemispheric Axonal Bifurcation of the Afferents to the Visual Cortical Areas during Postnatal Development in the Rat

Numerous cortical neurons in the juvenile and adult rat project to visual areas of both hemispheres whereas the vast majority of subcortical structures projecting to the visual cortex send strictly ipsilateral projections (Dreher et al., 1990). In the present study, the authors have sought to determine whether this pattern of axonal bifurcation in the connectivity of the visual areas undergoes a change during postnatal development. Two retrograde fluorescent dyes were used, fast blue (FB) and diamidino yellow (DY). Large multiple injections of one of the dyes were placed in all visual areas of one hemisphere and a small injection of the other dye was placed in area 17 of the opposite hemisphere. Labelled neurons were observed in subcortical and cortical structures on the side of the small injection. The experiments were performed on ten neonatal albino rat pups aged between 3 and 12 postnatal days (p.n.d.) at the time of injection and the results were compared with those obtained in the juvenile and adult animals, as reported in the preceding paper. In the thalamus of newborn animals, neurons belonging to nuclei located away from the midline send strictly ipsilateral cortical projections. However, in the midline nuclei of the intralaminar thalamic complex, a small region of overlap was observed between neurons projecting ipsilaterally and neurons projecting contralaterally in animals aged less than 9 postnatal days. In addition, in these neonatal animals a small number of bilaterally projecting neurons was detected in this region of overlap. In all other subcortical structures examined (ventral tegmental area, diagonal band of Broca, claustrum), the laterality of the projection was the same in the newborn and the adult animals. In particular, in the claustrum of neonatal animals, as in adult animals, there was a large contingent of contralaterally projecting neurons and only a very small number of bilaterally projecting neurons. The results in the cortex contrast with those observed in subcortical structures. Whereas ipsilaterally projecting neurons were distributed in a broadly similar way in newborn and adult animals, the laminar and areal distribution of contralaterally projecting neurons in newborn animals clearly differed from those observed in the adult animals. Furthermore, double labelled neurons were more numerous in animals aged less than 12 days than in adults. The proportions of such bilaterally projecting neurons were computed with respect to the numbers of neurons sending ipsilateral projections to area 17. These proportions are constant at all ages in the claustrum and cortical area 8. In areas 18a, 29 and 35 on the other hand, the proportions of bilaterally projecting neurons increase after 5 days and reach a peak in the period extending from 9 to 11 days of age when more than half of the neurons projecting ipsilaterally also send an axonal branch to the contralateral cortex. In cortical areas 29 and 35, this peak is followed by a sudden drop to the adult level at 12 postnatal days, whereas the return to the adult level is gradual in area 18a. These results demonstrate that, in subcortical structures and in cortical area 8, the laterality of the afferent connections to the visual cortex does not change during postnatal development. By contrast, cortical areas 18a, 29 and 35 go through a stage when numerous cells send bifurcating connections to both hemispheres. The timing of the decrease in proportions of bilaterally projecting neurons in these areas suggests that numerous neurons retract their callosal axonal branch when the adult pattern of callosal connectivity is established at 9 - 11 days of age.     

Cortical and thalamic afferent connections of the insular and adjacent cortex of the rat

Thalamic and cortical afferents to the insular and perirhinal cortex of the rat were investigated. Unilateral injections of horseradish peroxidase (HRP) were made iontophoretically along the rhinal sulcus. HRP injections covered or invaded areas along the rhinal fissure from about the level of the middle cerebral artery to the posterior end of the fissure. The most anterior injection labeled a few cells in the mediodorsal nucleus. More posterior injections labeled neurons in the basal portion of the nucleus ventralis medialis, thus suggesting that this cortical region constitutes the rat's gustatory (insular) cortex. We consider the cortex situated posterior to the gustatory cortex in and above the rhinal sulcus as the core region of the rat's (associative) insular cortex, as this cortex receives afferents from the regions of and between the nuclei suprageniculatus and geniculatus medialis, pars magnocellularis. It includes parts of the cortex termed perirhinal in other studies. The cortex dorsal and posterior to the insular cortex we consider auditory cortex, as it receives afferents from the principal part of the medial geniculate nucleus, and the cortex ventral to the insular cortex (below the fundus of the rhinal sulcus) we consider to constitute the prepiriform cortex, which is athalamic. The posterior part of the perirhinal cortex (area 35) receives afferents from nonspecific thalamic nuclei (midline nuclei). Cortical afferents to the injection loci arise from a number of regions, above all from regions of the medial and sulcal prefrontal cortex. Those injections confined to the projection cortex of the suprageniculate-magnocellular medial geniculate nuclear complex also led to labeling in contralateral prefrontal regions, particularly in area 25 (infralimbic region). A comparison of our results with those on the insular cortex of cats and monkeys suggests that on the basis of thalamocortical connections, topographical relations, and involvements of neurons in information processing and overt behavior, the insular cortex has to be regarded as a heterogeneous region which may be separated into prefrontal insular, gustatory (somatosensory) insular, and associative insular portions.     

Development of the rat septohippocampal projection: Tracing with DiI and electron microscopy of identified growth cones

The factors determining the development of specific fiber tracts in the central nervous system as well as the interactions of growth cones with the surrounding micromilieu are largely unknown. Here we investigated the ontogenetic development of the septohippocampal projection in the rat with the lipophilic carbocyanine dye DiI which is transported anterogradely and retrogradely in neurons and can be applied to fixed embryonic tissue. Photoconversion of anterogradely labeled fibers allowed us to study individual growth cones by electron microscopy. The first axons originating from the septal complex were found in the hippocampus as early as on embryonic day (ED) 19, reaching the fimbrial pole of the hippocampus on ED 18. However, on ED 17 we consistently found retrogradely labeled cells in the hippocampus, indicating that the development of the hippocamposeptal projection precedes that of the septohippocampal projection. On ED 19, the majority of the axons directed toward the hippocampal formation passed the hippocampus and grew further into the subicular complex and entorhinal cortex. These axons gave off collaterals that invaded the hippocampus proper. A fairly adult pattern of the septohippocampal projection was reached on postnatal day 10, although many growth cones were still found. A comparative analysis of individual growth cones found in the fimbria and the hippocampus proper revealed no striking differences in their morphology. Electron microscopic analysis showed that growth cones in the fimbria were mainly contacted by other axons, whereas growth cones in the hippocampus had contact with all available elements. This may indicate that growing septohippocampal fibers are guided by axons of the earlier formed hippocamposeptal projection. In the hippocampus proper, other cues, probably derived from the target itself, may guide the septhippocampal axons to their appropriate target cells. © 1993 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.     

Connections between the retrosplenial cortex and the hippocampal formation in the rat: a review.

The retrosplenial cortex is situated at the crossroads between the hippocampal formation and many areas of the neocortex, but few studies have examined the connections between the hippocampal formation and the retrosplenial cortex in detail. Each subdivision of the retrosplenial cortex projects to a discrete terminal field in the hippocampal formation. The retrosplenial dysgranular cortex (Rdg) projects to the postsubiculum, caudal parts of parasubiculum, caudal and lateral parts of the entorhinal cortex, and the perirhinal cortex. The retrosplenial granular b cortex (Rgb) projects only to the postsubiculum, but the retrosplenial granular a cortex (Rga) projects to the postsubiculu, rostral presubiculum, parasubiculum, and caudal medial entorhinal cortex. Reciprocating projections from the hippocampal formation to Rdg originate in septal parts of CA1, postsubiculum, and caudal parts of the entorhinal cortex, but these are only sparse projections. In contrast, Rgb and Rga receive dense projections from the hippocampal formation. The hippocampal projection to Rgb originates in area CA1, dorsal (septal) subiculum, and post-subiculum. Conversely, Rga is innervated by ventral (temporal) subiculum and postsubiculum. Further, the connections between the retrosplenial cortex and the hippocampal formation are topographically organized. Rostral retrosplenial cortex is connected primarily to the septal (rostrodorsal) hippocampal formation, while caudal parts of the retrosplenial cortex are connected with temporal (caudoventral) areas of the hippocampal formation. Together, the elaborate connections between the retrosplenial cortex and the hippocampal formation suggest that this projection provides an important pathway by which the hippocampus affects learning, memory, and emotional behavior.     

Fiber connections of the hippocampal formation and septum and subdivisions of the hippocampal formation in the pigeon as revealed by tract tracing and kainic acid lesions

The organization of the pigeon hippocampal formation was examined by tract tracing by using biotinylated dextran amine (BDA) and cholera toxin B subunit (CTB) and by injections of kainic acid to produce excitotoxic lesions. The hippocampal formation was divided into seven subdivisions based on Nissl staining and intrinsic and septal connections: dorsomedial (DM), dorsolateral (DL), triangular (Tr), V-shaped layer, magnocellular (Ma), parvocellular, and cell-poor regions. DL was composed of dorsal and ventral portions and sent associational fibers to DM, the V-shaped layer, and Tr. DL had strong reciprocal connections with the densocellular part of the hyperpallium (HD) and projected to the dorsolateral corticoid area. DM had reciprocal fiber connections with the V-shaped layer, Ma, and DL as well as with several subdivisions of the arcopallium. DL and DM, but not the V-shaped layer, projected fibers to the septum where those from DM exceeded in number those from DL. These projections further extended to the hypothalamus, particularly the lateral hypothalamic area. The lateral and medial septal nuclei projected back a very small number of ascending fibers to the hippocampal formation. Intraventricular injections of kainic acid induced neuronal loss widely in the hippocampal formation and subsequently produced gliosis in DM. These results indicate that DL receives its main afferents from HD and in turn sends inputs to an intrinsic circuit composed of hippocampal subdivisions DM, Ma, Tr, and the V-shaped layer; and also that DM is the main exit to the septum and hypothalamus. It is suggested that neurons in the V-shaped layer are intrinsic. Together, the results suggest that the V-shaped layer is comparable to the dentate gyrus of the mammalian hippocampal formation and that DM incorporates components comparable to both Ammon's horn and the subiculum.     

The Pontine A5 Noradrenergic Cells which Project to the Spinal Cord Dorsal Horn are Reciprocally Connected with the Caudal Ventrolateral Medulla in the Rat

A disynaptic pathway linking the caudal ventrolateral medulla (VLM) to the spinal cord via the A₅ noradrenergic cell group of the pons has recently been described in the rat. In the present work, the projections of the A₅ to the VLM and to the spinal dorsal horn were studied with double-tracing techniques combined with immunostaining of the noradrenaline-synthesizing enzyme dopamine-β-hydroxylase. Cholera toxin subunit B (CTb) injected into the VLM and fluoro-gold injected into the spinal dorsal horn produced double retrograde labelling of A₅ neurons immunoreactive for dopamine-β-hydroxylase, which received appositions of fibre varicosities labelled anterogradely with CTb injected into the VLM. After injecting CTb into the A₅, retrogradely labelled neurons occurred in the VLM. These neurons were contacted by anterogradely labelled fibres from the A₅ group. These observations indicate that the VLM cells acting upon the A₅ spinally projecting neurons, which are likely to exert an α₂-adrenoreceptor-mediated inhibition on the spinal cord, are targeted by collaterals of the A₅ spinal cord-bound axons. The A₅-VLM pathway may be the anatomical substrate of a negative feedback circuit whereby the modulatory action of the VLM on the spinal cord is self-inhibited through activation of the A₅.     

Projections from the parahippocampal region to the prefrontal cortex in the rat: evidence of multiple pathways

The purpose of the present study was to investigate, by means of anterograde tracing methods, the detailed organization of the parahippocampal-prefrontal projections in the rat brain. Efferents from the perirhinal cortex were found to terminate principally in both the ventromedial (prelimbic and infralimbic cortices) and lateral (agranular insular cortex) regions of the prefrontal cortex. Terminal fields were observed mainly in the superficial layers of the prefrontal cortex. Projections arising from the dorsolateral entorhinal cortex, which borders the perirhinal cortex along its ventral extent, were similarly directed to the ventromedial and lateral prefrontal cortices but also encompassed other frontal areas (dorsomedial and orbital prefrontal regions). Terminal fields of entorhinal projections were also found in the superficial layers of the prefrontal cortex. A third pathway, taking its source in the post-rhinal cortex, presented striking topographical differences with the two other output systems. Hence, post-rhinal efferences terminated only in the ventrolateral orbital area. The results indicate that two main routes originate from the parahippocampal region to reach the prefrontal cortex. One pathway involves the rostral and lateral portions of the parahippocampal region (perirhinal and dorsolateral entorhinal cortices), and the other relies on its most caudal region, the post-rhinal cortex. The presence of such different multiple parahippocampal-prefrontal pathways may have functional relevance for learning and memory processes.     

On the projections from the vestibular and perihypoglossal nuclei to the spinal trigeminal and lateral reticular nuclei in the cat

The projection from the vestibular and perihypoglossal nuclei to the spinal trigeminal and lateral reticular nuclei has been studied in cats where the wheat germ agglutinin-horseradish peroxidase complex has been used as a retrograde tracer. All injections were made at the level of the caudal pole of the inferior olive. The medial and descending vestibular, and the perihypoglossal nuclei were found to project to the spinal trigeminal nucleus. The projection to the lateral reticular nucleus reaches its medial-most part only, and originates in the lateral vestibular nucleus. The lateral part of the reticular formation also appears to be the target for some vestibular efferent fibres, mainly from the descending vestibular nucleus. The retrogradely labelled cells within the medial and descending vestibular nuclei are of all sizes and distributed throughout their entire territory. Certain observations furthermore indicate that the fibres reaching the lateral reticular nucleus are collaterals only from the vestibulospinal tract. The projections are bilateral. The observations confirm and extend previous observations on the afferent projections to the spinal trigeminal and lateral reticular nuclei.     

Projections from the anterodorsal and anteroveniral nucleus of the thalamus to the limbic cortex in the rat

The present study characterized the projections of the anterodorsal (AD) and the anteroventral (AV) thalamic nuclei to the limbic cortex. Both AD and AV project to the full extent of the retrosplenial granular cortex in a topographic pattern. Neurons in caudal parts of both nuclei project to rostral retrosplenial cortex, and neurons in rostral parts of both nuclei project to caudal retrosplenial cortpx. Within AV, the magnocellular neurons project primarily to the retrosplenial granular a cortex, whereas the parvicellular neurons project mainly to the retrosplenial granular b cortex. AD projections to retrosplenial cortex terminate in very different patternsthan do AV projections: The AD projection terminates with equal density in layers I, III, and IV of the retrosplenial granular cortex, whereas, in contrast, the AV projections terminate very densely in layer Ia and less densely in layer IV. Further, both AD and AV project densely to the postsubicular, presubicular, and parasubicular cortices and lightly to the entorhinal (only the most caudal part) cortex and to the subiculum proper (only the most septal part). Rostral parts of AD project equally to all three subicular cortices, whereas neurons in caudal AD project primarily to the postsubicular cortex. Compared to AD, neurons in AV have a less extensive projection to the subicular cortex, and this projection terminates primarily in the postsubicular and presubicular cortices. Further, the AD projection terminates in layers I, II/III, and V of postsubiculum, whereas the AV projection terminates only in layers I and V. © 1995 Wiley-Liss, Inc.     

Connections of the retrosplenial dysgranular cortex in the rat.

Although the retrosplenial dysgranular cortex (Rdg) is situated both physically and connectionally between the hippocampal formation and the neocortex, few studies have focused on the connections of Rdg. The present study employs retrograde and anterograde anatomical tracing methods to delineate the connections of Rdg. Each projection to Rdg terminates in distinct layers of the cortex. The thalamic projections to Rdg originate in the anterior (primarily the anteromedial), lateral (primarily the laterodorsal), and reuniens nuclei. Those from the anteromedial nucleus terminate predominantely in layers I and IV-VI, whereas the axons arising from the laterodorsal nucleus have a dense terminal plexus in layers I and III-IV. The cortical projections to Rdg originate primarily in the infraradiata, retrosplenial, postsubicular, and areas 17 and 18b cortices. The projections arising from visual areas 18b and 17 predominantly terminate in layer I of Rdg, axons from contralateral Rdg form a dense terminal plexus in layers I-IV, with a smaller number of terminals in layers V and VI, afferents from postsubiculum terminate in layers I and III-V, and the projection from infraradiata cortex terminates in layers I and V-VI. The efferent projections from Rdg are widespread. The major cortical projections from Rdg are to infraradiata, retrosplenial granular, area 18b, and postsubicular cortices. Subcortical projections from Rdg terminate primarily in the ipsilateral caudate and lateral thalamic nuclei and bilaterally in the anterior thalamic nuclei. The efferent projections from Rdg are topographically organized. Rostral Rdg projects to the dorsal infraradiata cortex and the rostral postsubiculum, while caudal Rdg axons terminate predominantely in the ventral infraradiata and the caudal postsubicular cortices. Caudal but not rostral Rdg projects to areas 17 and 18b of the cortex. The Rdg projections to the lateral and anterior nuclei also are organized along the rostral-caudal axis. Together, these data suggest that Rdg integrates thalamic, hippocampal, and neocortical information.     

Bidirectional connections of the medial amygdaloid nucleus in the Syrian hamster brain: Simultaneous anterograde and retrograde tract tracing

In the male Syrian hamster, mating is dependent on chemosensory and hormonal stimuli, and interruption of either input prevents copulation. The medial amygdaloid nucleus (Me) is a key nodal point in the neural circuitry controlling male sexual behavior because it relays both odor and steroid cues. Me is comprised of two major subdivisions, anterior (MeA) and posterior (MeP), which have distinct, although overlapping efferent projections. The present study investigated the afferents and efferents of MeA and MeP by using combined anterograde and retrograde tract tracing. Phaseolus vulgaris–leucoagglutinin and cholera toxin B were injected by iontophoresis through a single glass micropipette and detected by immunohistochemistry. MeA has widespread connections with olfactory structures, whereas MeP is heavily interconnected with steroid-responsive brain regions. The efferent projections of MeA and MeP were similar to those reported previously for the rat and hamster. In particular, MeP projects to the posteromedial subdivision of the bed nucleus of the stria terminalis (BNST) and to the medial preoptic nucleus, whereas MeA projects to adjacent subnuclei in BNST and the preoptic area. MeA and MeP also have distinct patterns of afferent input. Furthermore, the combination of anterograde and retrograde tract tracers shows that MeA and MeP are each bidirectionally connected with each other and with limbic nuclei. These results demonstrate that subnuclei of Me are interconnected with limbic structures in hamster brain. These connections may contribute to chemosensory and hormonal integration to control male sexual behavior. J. Comp. Neurol. 399:189–209, 1998. © 1998 Wiley-Liss, Inc.     

Organization of cortical and subcortical projections to anterior cingulate cortex in the cat

The aim of the experiments reported here was to identify cortical and subcortical forebrain structures from which anterior cingulate cortex (CGa) receives input in the cat. Deposits of retrograde tracers were placed at nine sites spanning the anterior cingulate area and patterns of retrograde transport were analyzed. Thalamic projections to CGa, in descending order of strength, originate in the anteromedial nucleus, lateroposterior nucleus, ventroanterior nucleus, rostral intralaminar complex, reuniens nucleus, mediodorsal nucleus, and laterodorsal nucleus. Minor and inconsistent ascending pathways arise in the paraventricular, parataenial, parafascicular, and subparafascicular thalamic nuclei. The basolateral nucleus of the amygdala, the hypothalamus, the nucleus of the diagonal band, and the claustrum are additional sources of ascending input. Cortical projections to CGa, in descending order of strength, derive from posterior cingulate cortex, prefrontal cortex, motor cortex (areas 4 and 6), parahippocampal cortex (entorhinal, perirhinal, postsubicular, parasubicular, and subicular areas), insular cortex, somesthetic cortex (areas 5 and SIV), and visual cortex (areas 7p, 20b, AMLS, PS and EPp). In general, the limbic, sensory, and motor afferents of CGa are weak. The dominant sources of input to CGa are other cortical areas with high-order functions. This finding calls into question the traditional characterization of cingulate cortex as a bridge between neocortical association areas and the limbic system.     

Severe tactual memory deficits in monkeys after combined removal of the amygdala and hippocampus

Monkeys with bilateral removals of both the amygdaloid complex and hippocampal formation were far more severely impaired on a tactual memory task than were monkeys with removal of either structure alone. These data parallel earlier findings on visual memory in monkeys and suggest that: (i) the memory deficit following combined ablations of the amygdala and hippocampus is multimodal; and (ii) the global anterograde amnesia observed in patients with medial temporal-lobe damage is also due to combined damage to these two structures.