Lamination and differential distribution of thalamic afferents within the sensory-motor cortex of the squirrel monkey

The structure of the first somatic sensory area (areas 3,1 and 2), of the motor area (area 4) and the intervening transitional field (area 3a) is described in the squirrel monkey (Saimiri sciureus) using Nissl, Bodian, Weil and Golgi preparations. The laminar arrangement of both cells and axons is briefly described and this is correlated with the Nauta and autoradiographic techniques. The latter method was used particularly in order to assess quantitative differences in the density of thalamic projections to the five cytoarchitectonic fields. In the somatic sensory areas thalamic afferents terminate not only in layer IV but to a large extent also in a recognizable part of layer III (layer IIIb). In area 4 thalamic terminals fill much of layer III, reaching almost to layer II. In area 3a the extent is intermediate between that seen in areas 3 and 4. It is thought that the extensive spread of thalamic terminals is related to the elongated form of a particular class of spine-bearing cell whose somata are situated in layer IV (Jones, 1975). In all areas a small proportion of thalamic afferents end also in layer I. Evidence is presented to indicate that specific afferent fibers emanating from the ventrobasal and ventrolateral complexes of the thalamus terminate in both the deep and superficial parts of layer I While “non-specific” afferents from other thalamic sources end in the superficial part. The autoradiographic studies indicate that there are considerable differences between the number of thalamic afferents ending in area 3 on the hand and in areas 1 and 2 on the other. Given this and the nature of the degenerating thalamic afferents observed in Nauta preparations, it is possible to identify thalamic afferents in normal Golgi preparations and significant differences are detectable in areas 4, 3 and 1 and 2. It is yet uncertain whether the slightly thinner, more sparsely distributed thalamic afferents ending in areas 1 and 2 are branches of those directed primarily to area 3.     

The organization of thalamic projections to the parietal cortex of the Virginia opossum

The right/left ratio for the number of neurons in individual pairs as well as series of pairs of normal rat and guinea pig thoracic dorsal root ganglia have been investigated. After perfusion of the animals with aldehyde fixatives, the 13 pairs of thoracic ganglia were embedded in resin, serially sectioned, and stained with azur methylene blue. Counts of neuronal nucleoli (with correction for possible split nucleoli) were used as an indicator of the number of neurons in each ganglion. In individual pairs the right/left difference varied between 0 and 47% in the rat and 0 and 26% in the guinea pig. There appeared to be no particular level with a preference for large right/left differences. However, when the total number of neurons from the 13 ganglia on one side were compared with the corresponding figure from the other side, the right/left differences were reduced to less than 3% in the rat and less than 2% in the guinea pig. These results show that the organization of the thoracic spinal nerve unit is markedly asymmetrical at the segmental level, but strictly symmetrical in terms of the total number of dorsal root ganglion cells. The marked asymmetry in individual ganglion pairs necessitates caution when evaluating the effect of unilateral experimental manipulations on the number of neurons in thoracic spinal ganglia.     

Size, laminar and columnar distribution of efferent cells in the sensory-motor cortex of monkeys.

The cells of origin of cortico-cortical and subcortical projections from the subfields of the somatic sensory area and from the motor cortex have been identified in cynomolgus and squirrel monkeys by the retrograde axonal transport method. The somata of the cells of origin of a particular fiber system have a specific laminar or sublaminar distribution. The somata of the majority of cortico-cortical cells lie in the supragranular layers. Those projecting to the opposite cortex are confined to the deeper half of layer III (layer IIIB). Ipsilateral cortico-cortical neurons lie mainly superficial to them in layers IIIA and II, but in the second somatic sensory area (SII) and in area 2 of the first (SI), small numbers are also found in layer V. Corticospinal cells lie in the deeper part of layer V and corticostriatal cells in the superficial part. Corticopontine, corticobulbar and corticorubral cells lie in between. The majority of corticothalamic cells lies in layer VI but a second, smaller population is found in the deep part of layer V. The cells giving rise to a particular set of efferent connections can be distinguished in terms of size and, with the exception of the corticospinal cells, their size does not vary greatly from area to area. In many cases, the size and laminar specificity indicates that cells sending axons to one site cannot have collateral branches projecting to another. In most of the fiber systems studied, labeled cells form single or multiple strips, 0.5–1 mm wide and oriented mediolaterally across the cortex. The strips appear in all of the subfields of the somatic sensory and motor areas and may form the basis of the clustering of like groups of efferent neurons demonstrable in physiological studies.     

The laminar distribution of intracortical fibers originating in the olfactory cortex of the rat

In this study, the autoradiographic method for tracing axonal connections was used to identify the laminar distribution of intracortical fibers originating in the olfactory cortical areas of the rat. Most of the projections can be divided into two major fiber systems with different laminar patterns of termination. The first of these, termed the layer Ib fiber system, arises in the anterior olfactory nucleus, the anterior and posterior piriform cortex, and the lateral entorhinal cortex, and terminates predominantly in layer Ib and, in many cases, layer III of the entire olfactory cortex. The second system, termed the layer II-deep Ib fiber system, originates in three relatively small olfactory cortical areas-the dorsal peduncular cortex, the ventral tenia tecta, and the periamygdaloid cortex and terminates in and around the cells of layer II in most parts of the olfactory cortex. There is significant overlap in the laminar distribution of the two systems, although the distinction between them is readily apparent. Within the layer Ib fiber system there are relatively slight but consistent differences in the lamination of fibers from different areas. The fibers from the anterior olfactory nucleus are concentrated in the deep part of layer Ib while those from the anterior piriform cortex are concentrated in the superficial part of this layer. The fibers from the posterior piriform cortex tend to be densest in the middle of layer Ib. These differences are maintained in all areas of termination of each set of fibers, both ipsilaterally and contra-laterally. In addition, intracortical fibers from the anterior cortical nucleus of the amygdala are distributed throughout layer I, including layer la and Ib. Fibers from the nucleus of the lateral olfactory tract terminate bilaterally around the cells of the islands of Callej a and the medial edge of the anterior piriform cortex.     

Receptive fields of thalamic neurons projecting to the motor cortex in the cat

The locations and receptive fields of thalamic neurons projecting to the motor cortex were examined and the following results were obtained. (1) Neurons located at the border area between nucleus ventralis lateralis (VL) and nucleus ventralis posterolateralis (VPL) could be activated antidromically from the motor cortex. (2) These neurons received topographically organized somesthetic inputs arising from skin and deep receptors. (3) The receptive fields of neurons in the small area of the motor cortex where these thalamic neurons projected could be examined in 8 instances. In 6 instances, the cortical neurons and the thalamic projection neurons were activated by exactly the same stimuli in the periphery. (4) Removal of the sensory cortex did not significantly change the characteristics of afferent inputs from the periphery to the motor cortex. (5) It is concluded that the motor cortex receives somesthetic inputs directly from the thalamus. The functional role of these inputs was discussed in relation to the known cortical reflexes.     

Spatial distribution and density of prefrontal cortical cells projecting to three sectors of the premotor cortex

The spatial distribution of prefrontal cortical cells projecting to three different sectors in the premotor cortex was examined. The cells projecting to the three sectors were distributed in separate regions in the dorsolateral prefrontal cortex with a small overlap. Cells projecting to the ventral sector were distributed in the lower bank of the principal sulcus (PS). Those projecting to the restro-dorsal sector were located near the superior limb of the arcuate sulcus, and in the dorsal convexity and upper bank of the PS. Cells projecting to the caudo-dorsal sector were observed in the upper bank of the PS and in the area 8a. These findings suggest that each of the three sectors of the premotor cortex receive different sets of information from the prefrontal cortex.     

Neuronal populations in the posterior group of thalamic nuclei projecting into the amygdaloid complex and auditory cortex in the cat

Location of neurons in posterior thalamic nuclei and neighbouring structures of the midbrain regions projecting to the amygdaloid complex and auditory cortex of cat was studied by the method of horseradish peroxidase. The main sources of these brain region projections to amygdaloid complex are peripeduncular , subparafascicular and suprageniculate nuclei and caudal division of the medial geniculate body. The cells of origin of projections to the auditory cortex are located in all medial geniculate nuclei and wide regions of the posterior thalamic group. Neuron pools projecting to the auditory cortex and amygdala exist in medial parts of the posterior thalamic nuclei. The role of posterior thalamic nuclei in transmission of auditory signals to amygdala is discussed.     

Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat

The organization of projections from the anterior thalamic nuclei to the cingulate cortex was analyzed in the rat by the anterograde transport of Phaseolus vulgaris-leucoagglutinin. The rostral part of the anteromedial nucleus projects to layers I, V and VI of the anterior cingulate areas 1 and 2, layers I and III of the ventral orbital area, layers I, V and VI of area 29D of the retrosplenial area, and layers I and V of the caudal part of the retrosplenial granular and agranular areas. In contrast, the caudal part of the anteromedial nucleus projects to layer V of the frontal area 2, and layers I and V of the rostral part of the retrosplenial granular and agranular areas. The interanteromedial nucleus projects to layers I, III and V of the frontal area 2, layer V of the agranular insular area, and layers I, V and VI of area 29D. The anteroventral nucleus projects to layers I and IV of the retrosplenial granular area, whereas the anterodorsal nucleus projects to layers I, III and IV of the same area. Projections from the anteroventral and anterodorsal nuclei were, furthermore, organized such that their ventral parts project to the rostral part of the retrosplenial granular area, whereas their dorsal parts project to the more caudal part. The results suggest that the anterior thalamic nuclei project to more widespread areas and laminae of the cingulate cortex than was previously assumed. The projections are organized such that the anteromedial and interanteromedial nuclei project to layer I and the deep layers of the anterior cingulate and retrosplenial cortex, whereas the anteroventral and anterodorsal nuclei project to the superficial layers of the retrosplenial cortex. These thalamocortical projections may play important roles in behavioral learning such as discriminative avoidance behavior.     

Cells of origin and terminal distribution of corticostriatal fibers arising in the sensory-motor cortex of monkeys.

The cells of origin of the corticostriatal projection have been identified in squirrel monkeys by the use of the retrograde horseradish peroxidase method. In the subfields of the somatic sensory, motor, parietal and frontal areas of the cortex, cells projecting to the ipsilateral striatum are relatively sparsely distributed and form a group of small- to medium-sized pyramidal cells with an average somal diameter from area to area of 14-16 mum. Such cells are found only in layer V of the cortex (mainly in the more superficial parts of the layer). Since they are consistently smaller than the pyramidal cells of layer V that project to the brainstem and spinal cord and since they lie outside layer VI which gives rise to corticothalamic axons, the corticostriatal axons are unlikely to be collaterals of axons projecting to other sites. The cells of origin of the crossed corticostriatal projection are also found in layer V and are pyramidal cells with somal diameters in the same range as above. They are found only in areas 4, 8, and 6. Studies with the anterograde, autoradiographic method in rhesus, cynomologous and squirrel monkeys, indicate that the somatic sensory areas project to most of the antero-posterior extent of the ipsilateral putamen. Subareas 3a, 3b, 1 and 2 of the somatic sensory cortex project to the same region and the projection overlaps similarly extensive projections from the motor and certain other areas of the cortex. However, in each case the pattern of terminal labeling is in the form of interrupted clusters, strips and bands. A single small injection of the cortex is associated with only one or two such clusters of terminal labeling. This seems to imply that individual corticostriatal fibers end in a very restricted manner and that the terminal ramifications of fibers from one cortical area may alternate in the putamen with those arising in other areas.     

Differential projections from the mediodorsal and centrolateral thalamic nuclei to the frontal cortex in rats

The aim of the present study was to investigate afferent projections from the medial thalamic nuclei (MT) to the frontal cortical areas using a single small iontophoretic injection of biotinylated dextran amine (BDA) and analysis of the anterogradely labeled fibers and varicosities. Projections from the mediodorsal (MD) nuclei were found primarily and extensively in the anterior cingulate cortex (ACC), whereas those from the centrolateral (CL) thalamic nucleus were found in the frontal motor cortex. The density of terminals in the ACC was high in layers II and III and sparse in layer I. The majority of projected fibers from the CL were found at a high density in layer V, with a moderate density in the superficial layers. The differential projection patterns were topographically organized in the medial prefrontal cortex and sensory motor cortex. These findings support the results of our previous electrophysiological studies suggesting that neurons in the medial thalamic nuclei relay nociceptive information to the limbic or sensory motor cortical areas. The present results agree with the current notion that the medial thalamo-frontal cortical network circuitry plays an important role in processing the emotional aspect of nociception.     

Organization of projections of rat retrosplenial cortex to the anterior thalamic nuclei

The organization of the projections from the retrosplenial cortex (Brodmann's area 29) to the anterior thalamic nuclei was examined in the rat with retrograde transport of the cholera toxin B subunit and anterograde transport of biotinylated dextran amine. Areas 29a and 29b project mainly ipsilaterally to the rostral two‐thirds of the anteroventral nucleus, with area 29a projecting more rostrodorsally than area 29b. Area 29c projects bilaterally to the ventromedial part of the anteroventral nucleus. The projections from area 29c are organized in a topographic pattern such that the rostral area 29c projects to the caudoventral part of the anteroventral nucleus, whereas the caudal area 29c projects to the more rostrodorsal parts. Caudal area 29d projects mainly ipsilaterally to the rostrodorsal part of the anteromedial nucleus, and the rostral and dorsal parts of the anteroventral nucleus, whereas rostral area 29d projects bilaterally to the caudodorsal part of the anteromedial nucleus and the caudolateral part of the anteroventral nucleus. All the areas of the retrosplenial cortex provide sparse projections, mainly ipsilateral, to the anterodorsal nucleus, with a crude topographic pattern such that the rostrocaudal axis of the retrosplenial cortex corresponds to the caudorostral axis of the anterodorsal nucleus. The results indicate that each area of the retrosplenial cortex has a distinct projection field within the anterior thalamic nuclei. This suggests that each of these projections transmits distinct information that is important for complex memory and learning functions, e.g. discriminative avoidance learning and spatial memory.     

Convergence of projections from various thalamic nuclei on the rat somatosensory cortex columns

The method of primuline fluorochrome retrograde transport was used to study sources of thalamo-cortical projections on a separate somatic cortical neuronal column connected with C3 vibrissae of albino rat. Labeled cells were found in 8 thalamic nuclei: tv, tvd, tpo, pf, rh, tvm, tvl, tr. The intensity of neuron staining and cell quantity and density varied in different nuclei. Hence their axon branching in the rat cortex was also different. The majority of intensively stained and densely packed cells have been observed in tv nucleus. The observed convergence of different thalamo-cortical inputs on single somatic cortex column explains heterogeneity in functional properties of the same column neurons and makes it possible for the column to form several neuronal assemblies with different functions.     

The subparafascicular thalamic nucleus of the rat receives projection fibers from the inferior colliculus and auditory cortex

The sources of afferent fibers to the subparafascicular thalamic nucleus (SPF) of the rat were investigated by the retrograde WGA-HRP and anterograde PHA-L methods. Layer V of the areas 3, 1 and 2 of the temporal cortex as well as the dorsal and external cortices of the inferior colliculus were found to send projection fibers to the whole rostrocaudal extent of the SPF bilaterally with a clear-cut ipsilateral dominance. The results indicate that the SPF of the rat may constitute a relay nucleus in the central auditory pathways.     

Cerebellopontine projections in the American opossum. A study of their origin, distribution and overlap with fibers from the cerebral cortex

The origin, course and distribution of cerebellopontine fibers was studied in the opossum by employing the Nauta-Gygax and Fink-Heimer techniques. Our results substantiate and extnd those of Brodal, Destombes, Lacerda and Angaut ('72) concerning the existence of cerebellopontine projections and provide evidence for a hitherto unreported fastigial projection to the basilar pons. Destruction of the caudal, medial division of the fastigial nucleus elicits bilateral degeneration in a restricted area of the medial pontine nucleus. This small terminal field is located in the angle between the medial lemniscus and the pyramidal tract and is found throughout the caudal three-fifths of the pons. The degenerating fibers do not course within the descending brachium conjunctivum, but reach the pons by filtering through the reticular formation from the uncinate fasciculus. Lesions that involve either the interpositus anterior or the dentate nucleus produce degeneration within the contralateral descending brachium conjunctivum and basilar pons. Terminal fields are located within the median, medial (paramedian nucleus of cat), peduncular, ventral and lateral nuclei. The heaviest degeneration is in the medial nucleus. Although cerebellar and cortical projections have different targets in the basilar pons, there is some overlap. Fastigial and preorbital fibers have partial overlap in the dorsal part of the medial nucleus, whereas the peduncular and lateral nuclei are the areas of overlap between the interpositus anterior and dentate projections with those from forelimb (and probably face) cortical areas. This overlap is particularly obvious in the caudal part of the lateral nucleus and occurs between fibers from limb motor-sensory cortex and those arising mainly within the anterior interpositus nucleus. There is no pontine overlap between cerebellar and visual or auditory cortical projections.