Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum

The afferent connections of the insula in the rhesus monkey were studied with axonal transport methods. Injections of horseradish peroxidase (HRP) in the insula revealed labeled neurons in the prefrontal cortex, the lateral orbital region, the frontopariefal operculum, the cingulate gyrus and adjacent medial cortex, the prepiriforrn olfactory cortex, the temporal pole, the cortex of the superior temporal sulcus, the rhinal cortex, the supratem-poral plane, and the posterior parietal lobe. Tritiated amino acid (TAA) injections in some of the cortical regions which contained retrogradely labeled neurons confirmed projections to the insula from prefrontal granular cortex, orbital frontal cortex, prepiriform cortex, temporal pole, rhinal cortex, cingulate gyrus, frontal operculum, and parietal cortex. In these studies, cortical areas that projected to the insula also projected to the claustrum. However, the topographic and quantitative relationships between the projections into the insula and those into the claustrum were inconsistent. Moreover, the claustrum has additional connections which it does not share with the insula. A selected review of the literature suggests that the claustrum and insula differ widely also with respect to ontogenesis and functional specialization.     

Efferent cortical connections of multimodal cortex of the superior temporal sulcus in the rhesus monkey.

The cortex of the upper bank of the superior temporal sulcus (STS) in the rhesus monkey contains a region that receives overlapping input from post-Rolandic sensory association areas and is considered multimodal in nature. We have used the fluorescence retrograde tracing technique in order to answer the question of whether multimodal areas of the STS project back to post-Rolandic sensory association areas. Additionally, we have attempted to answer the question of whether the projections from the multimodal areas directed to the parasensory association areas originate from common neurons via axon collaterals or from individual neurons. The results show that multimodal area TPO of the STS projects back to specific unimodal parasensory association areas of the parietal lobe (somatosensory), superior temporal gyrus (auditory), and posterior parahippocampal gyrus (visual). In addition, a substantial number of projections from area TPO are directed to distal parasensory association areas, area PG-Opt in the inferior parietal lobule, areas Ts1 and Ts2 in the rostral superior temporal gyrus, and areas TF and TL in the parahippocampal gyrus. These latter regions are themselves considered to be higher-order association areas. It was also noted that the majority of the projections to these higher-order association areas originate from the middle divisions of area TPO (TPO-2 and TPO-3). These neurons are organized in a significantly overlapping manner. Despite this overlap of the projection neurons, only an occasional double labeled neuron was observed in area TPO. Thus, our observations indicate that the multimodal region of the superior temporal sulcus has reciprocal connections with the unimodal parasensory association cortices subserving somatosensory, auditory and visual modalities, as well as with other post-Rolandic higher-order association areas. These connections from area TPO to post-Rolandic association areas may have a modulating influence on the sensory association input leading to multimodal areas in the superior temporal sulcus.     

Projections of the parabrachial nucleus in the old world monkey

The efferent projections of the pontine parabrachial nucleus (PBN) were examined in the Old World monkey (Macaca fascicularis) using tritiated amino acid autoradiography and horseradish peroxidase histochemistry. Parabrachiofugal fibers ascended to the forebrain along three pathways: the central tegmental tract, the ventral ascending catecholaminergic pathway, and a pathway located on the midline between the medial longitudinal fasciculi. The PBN projected heavily to the central nucleus of the amygdala and the lateral division of the bed nucleus of the stria terminalis and moderately to the ventral tegmental area and the substantia nigra. Light terminal label also was present within the dorsomedial, ventromedial, lateral, supramammillary, and infundibular nuclei of the hypothalamus and the annular nucleus and the dorsal raphe nucleus within the brain stem. The overall pattern of terminal label was similar to that previously reported for nonprimate species, but several differences were notable. In monkey the projection to the ventrobasal thalamus did not coincide with the region that contains gustatory-responsive neurons. In rats, these parabrachiothalamic fibers convey gustatory activity but in the monkey these fibers may carry visceral afferent information. The projections from the PBN to the hypothalamus in the monkey were neither as widespread nor as intense as in the rat, and the monkey lacks a projection from the PBN to the frontal and insular cortices.     

The posterior thalamic region and its cortical projection in new world and old world monkeys

The posterior nuclear complex of the thalamus in rhesus, pigtailed and squirrel monkeys consists of the combined suprageniculate-limitans nucleus and an ill defined region of heterogeneous cell types extending anteriorly from the dorsal lobe of the medial geniculate body towards the posterior pole of the ventral nuclear complex. This region is referred to as the posterior nucleus. The cortical projections of each of these nuclei, together with those of the adjacent ventral, pulvinar and medial geniculate complexes, have been studied by means of the autoradiographic tracing technique. The suprageniculate-limitans nucleus, the main input to which is the superior colliculus, projects upon the granular insular area of the cortex. The medial portion of the posterior nucleus projects to the retroinsular field lying posterior to the second somatic sensory area. There is clinical and electrophysiological evidence to suggest that the retroinsular area may form part of a central pain pathway. The lateral portion of the posterior nucleus which is closely related to certain elements of the medial geniculate complex, projects to the postaditory cortical field. The ventroposterioinferior nucleus, which may be involved in vestibular function, projects to the dysgranular insular field. The principal medial geniculate nucleus can be subdivided into a ventral division that projects to field AI of the auditory cortex and a dorsal division that merges with the posterior nucleus; it is further subdivided into an anterodorsal component that projects to two fields on the superior temporal gyrus, together with a posterodorsal component in which separate cell populations project to areas lying anterior and medial to AI. The magnocellular medial geniculate nucleus, sometimes considered a part of the posterior complex, appears to project diffusely to layer I of all the auditory fields. The Auditory fields are bounded on three sides by the projection field of the medial nucleus of the pulvinar which also extends into the upper end of the lateral sulcus to bound the fields receiving fibers from the posterior nucleus. The topography of the areas receiving fibers from the posterior, medial geniculate and pulvinar complexes, taken in conjunction with the rotation of the primate temporal lobe, permits all of these fields to be compared with similar, better known areas in the cat brain.     

Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections.

In this investigation the efferent projections of the entorhinal and prorhinal cortices relative to their sites of termination in the hippocampus and fascia dentata were investigated in the rhesus monkey using experimental silver impregnation methods. Contrary to the often cited observations of Lorente de No, all entorhinal areas, including the laterally lying prorhinal cortex, were found to give rise to the perforant pathway, and furthermore, each cytoarchitectonically defined subarea was found to contribute a unique component. These perforant pathway components terminate in distinct regions of the dendritic zones of the fascia dentata granule cell and the hippocampal pyramidal cell. A previously undescribed projection to the prosubiculum and hippocampus has been found to originate from the prorhinal cortex which forms the medial wall of the rhinal sulcus along the lateral-most portion of the entorhinal cortex in the rhesus monkey. These results, in conjunction with our previous observations regarding differential afferents to the entorhinal cortex, indicate that specific afferent and efferent connections characterize each cytoarchitectonically definable subareas of this periallocortical region. Additionally, they indicate that the perforant pathway might be conceptualized as the final link in a multisynaptic series of connections instrumental in providing the hippocampus with potential modality specific and multimodal input.     

Septal complex of the telencephalon of lizards: III. Efferent connections and general discussion

The projections of the septum of the lizard Podarcis hispanica (Lacertidae) were studied by combining retrograde and anterograde neuroanatomical tracing. The results confirm the classification of septal nuclei into three main divisions. The nuclei composing the central septal division (anterior, lateral, medial, dorsolateral, and ventrolateral nuclei) displayed differential projections to the basal telencephalon, preoptic and anterior hypothalamus, lateral hypothalamic area, dorsal hypothalamus, mammillary complex, dorsomedial anterior thalamus, ventral tegmental area, interpeduncular nucleus, raphe nucleus, torus semicircularis pars laminaris, reptilian A8 nucleus/ substantia nigra and central gray. For instance, only the medial septal nucleus projected substantially to the thalamus whereas the anterior septum was the only nucleus projecting to the caudal midbrain including the central gray. The anterior and lateral septal nuclei also differ in the way in which their projection to the preoptic hypothalamus terminated. The midline septal division is composed of the dorsal septal nucleus, nucleus septalis impar and nucleus of the posterior pallial commissure. The latter two nuclei projected to the lateral habenula and, at least the nucleus of the posterior pallial commissure, to the mammillary complex. The dorsal septal nucleus projected to the preoptic and periventricular hypothalamus and the anterior thalamus, but its central part seemed to project to the caudal midbrain (up to the midbrain central gray). Finally, the ventromedial septal division (ventromedial septal nucleus) showed a massive projection to the anterior and the lateral tuberomammillary hypothalamus. Data on the connections of the septum of P. hispanica and Gecko gekko are discussed from a comparative point of view and used for better understanding of the functional anatomy of the tetrapodian septum. J. Comp. Neurol. 401:525–548, 1998. © 1998 Wiley-Liss, Inc.     

Efferent subcortical projections of the laryngeal motorcortex in the rhesus monkey

In order to better understand the descending voluntary vocal control pathway, the efferent subcortical projections of the laryngeal motorcortex were studied in the rhesus monkey (Macaca mulatta). For this purpose, the left motorcortex was exposed in three animals under narcosis. By electrical brain stimulation, sites were identified yielding vocal fold adduction. Effective sites were injected with the anterograde tracer biotin dextran amine. Subcortical projections could be traced within the forebrain to the putamen, caudate nucleus, claustrum, zona incerta, field H of Forel and a number of thalamic nuclei, with the heaviest projections to the nuclei ventralis lateralis, ventralis posteromedialis, including its parvocellular part, medialis dorsalis, centralis medialis, centrum medianum and reuniens. In the midbrain, labeling was found in the deep mesencephalic nucleus. In the lower brainstem, fibers terminated in the pontine and medullary reticular formation, locus coeruleus, nucleus subcoeruleus, medial parabrachial nucleus, nucleus of the spinal trigeminal tract, solitary tract nucleus and facial nucleus. No projections were found to the nucl. ambiguus. The fact that monkeys, in contrast to humans, lack a direct connection of the motorcortex with the laryngeal motoneurons suggests that this connection has evolved in the last few million years and might represent one of the factors that made speech evolution possible.     

Neurochemical gradients along monkey sensory cortical pathways: calbindin-immunoreactive pyramidal neurons in layers II and III

We examined the distribution of neurons containing immunoreactivity for three calcium-binding proteins, calbindin, parvalbumin and calretinin, as well as nonphosphorylated neurofilament protein, in cortical areas along the ventral and dorsal cortical visual pathways, and in ventrally-directed somatosensory and auditory cortical pathways. Calbindin-immunoreactive pyramidal neurons showed the most prominent regional differences. They were largely restricted to layers II and III and their number monotonically increased from the primary sensory areas to the anteroventral areas along the ventral visual pathway and along the ventrally-directed somatosensory and auditory pathways. The number of calbindin-immunoreactive pyramidal neurons in layers II and III also increased along the dorsal visual pathway, but the number in the last recognized stage of the dorsal visual pathway (area 7a) was significantly smaller than that at the corresponding stage in the ventral visual pathway (TE). The number of calbindin-immunoreactive pyramidal neurons was highest in layers II and III of areas 35/36, TG, and TF/TH, which represent terminal cortical regions of the pathways. These results show neurochemical differences between cortical areas located at early and late stages along serial corticocortical pathways, as well as confirming differences between pyramidal neurons in the supragranular and infragranular layers.     

The entorhinal cortex of the monkey: III. Subcortical afferents

The subcortical afferent connections of the entorhinal cortex of the Macaca fascicularis monkey were investigated by the placement of small injections of the retrograde tracer wheat germ agglutinin conjugated to horseradish peroxidase into each of its subdivisions. Retrogradely labeled cells were observed in several subcortical regions including the amygdaloid complex, claustrum, basal forebrain, thalamus, hypothalamus, and brainstem. In the amygdala, labeled cells were observed principally in the lateral nucleus, the accessory basal nucleus, the deep or paralaminar portion of the basal nucleus, and the periamygdaloid cortex. Additional retrogradely labeled cells were found in the endopiriform nucleus, the anterior amygdaloid area, and the cortical nuclei. Retrogradely labeled cells were observed throughout much of the rostrocaudal extent of the claustrum and tended to be located in its ventral half. In the basal forebrain, retrogradely labeled cells were observed in the medial septal nucleus, the nucleus of the diagonal band, and to lesser extent within the substantia innominata. Several of the cells in the latter region were large and located within the densely packed neuronal clusters of the basal nucleus of Meynert. Most of the labeled cells in the thalamus were located in the midline nuclei. Many were found in nucleus reuniens, but even greater numbers were located in the centralis complex. Additional labeled cells were located in the paraventricular and parataenial nuclei. In all cases, numerous retrogradely labeled cells were observed in the medial pulvinar. In the hypothalamus, most of the retrogradely labeled cells were located in the supramamillary area, though scattered cells were also observed in the perifornical region and in the lateral hypothalamic area. Caudal to the mamillary nuclei there were labeled cells in the ventral tegmental area. There were relatively few labeled cells in the brainstem and these were invariably located either in the raphe nuclei or locus coeruleus.     

Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a PHA-L study of subcortical projections.

The subcortical projections of the centromedian (CM) and the parafascicular (Pf) thalamic nuclei were examined in the squirrel monkey (Saimiri sciureus) by using the lectin Phaseolus vulgaris-leucoagglutinin (PHA-L) as an anterograde tracer. Both CM and Pf project massively to the striatum where they arborize in a complementary fashion. On the one hand, CM innervates most of the putamen caudal to the anterior commissure, a dorsolateral rim of the putamen rostral to the anterior commissure, discrete areas of the head of the caudate nucleus close to the internal capsule, and a lateral sector of the body of the caudate nucleus. On the other hand, Pf provides a heavy input to the head, body, and tail of the caudate nucleus, and to the rostral putamen, excluding the areas innervated by CM. In addition, Pf projects more discretely to the nucleus accumbens and the olfactory tubercle. Therefore, the projections from both CM and Pf cover the entire striatum, with those from CM arborizing into the "sensorimotor" striatal territory and the ones from Pf innervating the "associative-limbic" striatal territory. Furthermore, CM and Pf project to extrastriatal subcortical structures, such as the globus pallidus, the subthalamic nucleus, and the substantia nigra, where they also terminate in a complementary fashion. Topographically and cytologically, Pf is closely related to the subparafascicular nucleus (sPf). The Pf-sPf complex projects to the hypothalamus, the substantia innominata, the peripeduncular nucleus, and the amygdala. It also gives rise to descending efferents arborizing in various brainstem structures, including the inferior olivary complex. Additional studies with retrograde double-labeling methods show that distinct cell groups within CM project to the motor cortex and the striatum. Likewise, separate neuronal populations within the CM-Pf-sPf complex give rise to striatal and brainstem projections, the former arising from CM and Pf and the latter mainly from sPf. The complementary nature of CM and Pf projections to the striatum and other basal ganglia components suggests that this thalamic complex participates in a highly ordered manner in the parallel processing of the information that flows through the basal ganglia.     

Macaque monkey retrosplenial cortex: III. Cortical efferents

We have investigated the cortical efferent projections of the macaque monkey retrosplenial and posterior cingulate cortices by using (3)H-amino acids as anterograde tracers. All the injections produced extensive local connections to other portions of this region. There were also a number of extrinsic efferent cortical connections, many of which have not hitherto been reported. Major projections from the retrosplenial cortex were directed to the frontal lobe, with heaviest terminations in areas 46, 9, 10, and 11. There were also very substantial projections to the entorhinal cortex, presubiculum, and parasubiculum of the hippocampal formation, as well as to areas TH and TF of the parahippocampal cortex. Some injections led to labeling of area V4, the dorsal bank of the superior temporal sulcus, and area 7a of the parietal cortex. Projections from the posterior cingulate cortex innervated all these same regions, although the density of termination was different from the retrosplenial projections. The posterior cingulate cortex gave rise to additional projections to parietal area DP and to the cortex along the convexity of the superior temporal gyrus. The ventral portion of the posterior cingulate cortex (area 23v) gave rise to much denser efferent projections to the hippocampal formation than the dorsal portions (areas 23e and i). These connections are discussed in relation to the clinical syndromes of retrosplenial amnesia and topographic disorientation in humans commonly caused by lesions in the caudoventral portions of the retrosplenial and posterior cingulate cortices.     

Entorhinal cortex of the monkey: IV. Topographical and laminar organization of cortical afferents

The nonhuman primate entorhinal cortex is the primary interface for information flow between the neocortex and the hippocampal formation. Based on previous retrograde tracer studies, neocortical afferents to the macaque monkey entorhinal cortex originate largely in polysensory cortical association areas. However, the topographical and laminar distributions of cortical inputs to the entorhinal cortex have not yet been comprehensively described. The present study examines the regional and laminar termination of projections within the entorhinal cortex arising from different cortical areas. The study is based on a library of 51 (3)H-amino acid injections that involve most of the afferent regions of the entorhinal cortex. The range of termination patterns was broad. Some areas, such as the medial portion of orbitofrontal area 13 and parahippocampal areas TF and TH, project widely within the entorhinal cortex. Other areas have a more focal and regionally selective termination. The lateral orbitofrontal, insular, anterior cingulate, and perirhinal cortices, for example, project only to rostral levels of the entorhinal cortex. The upper bank of the superior temporal sulcus projects mainly to intermediate levels of the entorhinal cortex, and the parietal and retrosplenial cortices project to caudal levels. The projections from some of these cortical regions preferentially terminate in the superficial layers (I-III) of the entorhinal cortex, whereas others project more heavily to the deep layers (V-VI). Thus, some of the cortical inputs may be more influential on the cortically directed outputs of the hippocampal formation or on gating neocortical information flow into the other fields of the hippocampal formation rather than contributing to the perforant path inputs to other hippocampal fields.     

Efferent connections of the internal globus pallidus in the squirrel monkey: I. topography and synaptic organization of the pallidothalamic projection

The objectives of this study were, on one hand, to better understand how the segregated functional pathways from the cerebral cortex through the striatopallidal complex emerged in the projections to the thalamus and, on the other hand, to compare the ultrastructure and synaptic organization of the pallidal efferents to the ventrolateral (VL) and centromedian (CM) thalamic nuclei in primates. These aims were achieved by injections of the retrograde-anterograde tracer, biotinylated dextran amine (BDA), in different functional regions of the internal pallidum (GPi) in squirrel monkeys. The location of retrogradely labelled cells in the striatum was determined to ascertain the functional specificity of the injection sites. Injections in the ventrolateral two-thirds of the GPi (group 1) led to retrograde labelling in the postcommissural region of the putamen (“sensorimotor striatum”) and plexuses of labelled fibers in the rostral one-third of the principal ventrolateral nucleus (VLp) and the central part of the CM. On the other hand, injections in the dorsal one-third (group 3) and the rostromedial pole (group 4) of the GPi led to retrogradely labelled cells in the body of the caudate nucleus (“associative striatum”) and the ventral striatum (“limbic striatum”), respectively. After those injections, dense plexuses of anterogradely labelled varicosities were found in common thalamic nuclei, including the parvocellular ventral anterior nucleus (VApc), the dorsal VL (VLd), and the rostrodorsal part of the parafascicular nucleus (PF). In the caudal two-thirds of the CM/PF, the labelled fibers formed a band that lay along the dorsal border of the complex in a region called the dorsolateral PF (PFdl) in this study. The ventromedial nucleus (VM) was densely labelled only after injections in the rostromedial GPi, whereas the dorsal part of the zona incerta was labelled in both groups. At the electron microscopic level, the BDA-positive terminals in the VLp were larger and more elongated than those in the CM but, overall, displayed the same pattern of synaptic organization. Our findings indicate 1) that some associative and limbic cortical information, which is largely processed in segregated corticostriatopallidal channels, converges to common thalamic nuclei and 2) that the PF is a major target of associative and limbic GPi efferents in monkeys. J. Comp. Neurol. 382:323-347, 1997. © 1997 Wiley-Liss, Inc.     

Efferent connections of the red nucleus in the brainstem and spinal cord of the Rhesus monkey

Three types of neuron with differences in Nissl pattern were found in the red nucleus of the rhesus monkey. Neurons with coarse Nissl bodies occurred only in the caudal third of the red nucleus except for a small number which extended rostrally a short distance along the dorsolateral margin. Neurons with fine Nissl bodies occupied the rostral two-thirds of the nucleus. Neurons with slight cytoplasmic basophilia (achromatic) were smaller than the other types and distributed throughout the red nucleus. Perikaryal areas of the coarse and fine neurons, measured with a computer, had widely overlapping distributions. Electrolytic lesions were made unilaterally in the red nucleus of nine monkeys. Ascending axonal degeneration was studied in sections stained by the Fink-Heimer method. Two separate descending tracts were followed. The rubrobulbo-spinal tract took origin from coarse neurons, crossed completely in the ventral tegmental decussation, and terminated as follows: in parts of the superior sensory trigeminal, motor facial and lateral reticular nuclei; in the gracile and cuneate nuclei; in the nucleus medullae oblongata, subnucleus dorsalis; in Rexed's laminae V, VI, VII at all levels of the spinal cord. In contrast, the rubroreticulo-olivary tract took origin from fine neurons, remained uncrossed, and terminated in some reticular nuclei (pedunculopontine, pontis oralis and caudalis, gigantocellularis) and in parts of the inferior olivary complex. Degeneration was profuse in the dorsal lamina of the main olive, abundant in the ventral lamina, particularly in its lateral side, sparse and inconstant in the medial accessory olive, and invariably absent in the dorsal accessory olive. Thus, nuclei which receive descending projections from the red nucleus may be grouped into those with connections to lower motor neurons, cerebellum, or thalamus.     

Prefrontal granular cortex of the rhesus monkey. I. Intrahemispheric cortical afferents.

In 6 adolescent rhesus monkeys, unilateral injections of horseradish peroxidase (HRP) were made into 6 regions on the convexity of the prefrontal granular cortex.The afferents to each zone were considered with respect to whether they were local afferents (from adjacent frontal areas) or distal afferents (from outside frontal lobe). The strongest input onto prefrontal granular cortex comes from the temporal lobe and especially areas in and around the superior temporal gyrus. Area 10 in the frontal pole region receives input primarily from area 22 in the superior temporal gyrus and dorsal portion of the superior temporal sulcus. That portion of area 46 above the principal sulcus receives input primarily from area 22 in the upper bank of the superior temporal sulcus while area 46 below the principal sulcus has input from the insula of the superior temporal sulcus and area 21 in the lower bank of the superior temporal sulcus. The cortex within the concavity of the acurate sulcus differs in that the dorsal half (including areas 46 and 8a) receives input primarily from the dorsal bank and to a lesser degree the insula of the superior temporal sulcus while the ventral portion of this region including areas 45 and 46 receives input primarily from the lower bank of the superior temporal sulcus, inferior temporal gyrus and insula of the superior temporal sulcus. Input was noted from cingulate areas 23 and 24 to all 6 injected regions while retrosplenial cortex was noted to project to all but one of the injected regions, i.e. area 10. In addition, some labeled neurons were seen in area 7 after injections into area 46 and some were also seen in the inferior temporal gyrus and parahippocampal region after injections into the arcuate region. Finally, labeled neurons were noted in area 19 after injections into the ventral portion of the prefrontal granular cortex bounded by the arcuate sulcus.The HRP-positive neurons that comprised the intrahemispheric cortical afferents to prefrontal granular cortex were located primarily in layer iii. They were pyramidal in shape and ranged in size from small to medium. These neurons were found to be distributed in a horizontal band in which the number of labeled neurons waxed and waned, or they were distributed in a patchy or clumped manner. The possibility that both patterns of distribution represent a vertical or columnar organization to these afferent neurons is discussed.     

Prefrontal granular cortex of the rhesus monkey. II. Interhemispheric cortical afferents.

In 6 adolescent rhesus monkeys, horseradish peroxidase (HRP) was injected into 6 regions of the dorsalateral convexity of the prefrontal granular cortex. The commissural connections originated in both homotopical and heterotopical zones of the hemisphere contralateral to the injection site. The areas affected by the injections, i.e. areas 46,45, 10, 9, 12 and 8a, received extensive homotopical interhemispheric input. HRP-labeled neurons were less extensive in heterotopical as opposed to homotopical cortex but they were seen in all 6 cases and were most common in prefrontal areas and less common in cingulate areas, areas 21 and 22 in the superior temporal sulcus and in insular cortex. The cells, whether of heterotopical or homotopical origin, were located primarily in layer III. The most common distribution pattern was a horizontal band of HRP-labeled neurons which waxed and waned in cell density especially in homotopical cortex or patches and clusters of labeled cells especially in heterotopical cotex. This waxing and waning and grouping of neurons in pathces and clusters may well represent a vertical type of organization to the neurons which give rise to the interhemispheric cortical afferents to prefrontal granular cortex in the monkey.