Contralateral thalamic projections predominantly reach transitional cortices in the rhesus monkey

Connections between the thalamus and the cortex are generally regarded as ipsilateral, even though contralateral connections exist as well in several adult mammalian species. It is not known however, whether contralateral thalamocortical projections reach particular cortices or whether they emanate from specific nuclei. In the rhesus monkey different types of cortices, ranging from transitional to eulaminate, vary in their cortical connectional pattern and may also differ in thier thalamic connections. Because olfactory and transitional prefrontal cortices receive widespread projections, we investaged whether they are the target of projections from the contralateral thalamus as well. With the aid of retrograde tracers, we studied the thalamic projections of primary olfactory (olfactory tubercle and prepiriform cortex) and transitional orbital (areas PAPP, Pro 13) and medial (areas 25, 24, 32) areas, and of eulaminate (areas 11, 12, 9) cortices for comparison. To determine the prevalence of neurons in the contralateral thalamus, we compared them with the ipsilateral in each case. The pattern of ipsilateral thalamic projections differed somewhat among orbital, medial, and olfactory cortices. The mediodorsal nucleus was the predominant source of projections to orbital areas, midline nuclei included consistently about 25% of the thalamic neurons directed to medial transitional cortices, and primary olfactory areas were distinguished by receiving thalamic projections predominantly from neurons in midline and intralaminar nuclei. Notwithstanding some broad differences in the ipsilateral thalamofrontal projections, which appeared to depend on cortical location, the pattern of contralateral projections was thalamus were noted in midline, the magnocellular sector of the mediodorsal nucleus, the anterior medial and intralaminar nuclei, and ranged from 0 to 14% of the ipsilateral; they were directed primarily to olfactory and transitional orbital and medical cortices but rarely projected to eulaminate areas. Several thalamic nuclei projected from both sides to olfactory and transitional areas, but issued only ipsilateral projections to eulaminate areas. Though ipsilateral thalamocortical projections predominate in adult mammalian species, crossed projections are a common feature in development. The results suggest differences in the persistence of contralateral thalamocortical interactions between transitional and eulaminate cortices. © 1994 Wiley-Liss, Inc.     

Architectural subdivisions of medial and orbital frontal cortices in the marmoset monkey (Callithrix jacchus)

Although the common marmoset has become a model for the study of several neurological conditions that affect the frontal lobe, knowledge of the boundaries of the areas located in the orbital and medial frontal regions has remained incomplete. Here we examined histological sections stained for myelin, Nissl substance, and cytochrome oxidase, allowing identification of likely homologues of most of the architectural fields defined in Old World monkeys. Ventrally, we identified three granular fields at or near the frontal pole (area 10, and the medial and lateral subregions of area 11), and two granular fields along the lateral margin of the orbitofrontal cortex (medial and orbital subdivisions of area 12). More caudal and medially, dysgranular and agranular cortices included four subdivisions of area 13 as well as rostral and caudal subdivisions of area 14 (at the ventromedial convexity). The ventral frontotemporal transition encompassed at least two subdivisions of agranular insular cortex, as well as the likely homologues of the gustatory cortices. Most of the medial surface was encompassed by area 10 (which projected a caudomedial finger‐like extension toward the subgenual cortex), together with a relatively large dysgranular area 32 and an agranular area 25 (in subgenual cortex). Finally, the caudal limit of the medial frontal cortex included two fields of agranular cingulate cortex (areas 24a and 24b). These findings enhance our understanding of the architectural organization of the marmoset frontal cortex and highlight a highly conserved basic organization across simian primates, allowing the informed interpretation of experimental neurological studies. J. Comp. Neurol. 514:11–29, 2009. © 2009 Wiley‐Liss, Inc.     

Cytoarchitectonic subdivisions of the dorsolateral frontal cortex of the marmoset monkey (Callithrix jacchus), and their projections to dorsal visual areas

We describe the organization of the dorsolateral frontal areas in marmoset monkeys using a combination of architectural methods (Nissl, cytochrome oxidase, and myelin stains) and injections of fluorescent tracers in extrastriate areas (the second visual area [V2], the dorsomedial and dorsoanterior areas [DM, DA], the middle temporal area and middle temporal crescent [MT, MTc], and the posterior parietal cortex [area 7]). Cytoarchitectural field 8 comprises three subdivisions: 8Av, 8Ad, and 8B. The ventrolateral subdivision, 8Av, forms the principal source of frontal projections to the "dorsal stream," having connections with each of the injected visual areas. The cytoarchitectural characteristics of 8Av suggest that this subdivision corresponds to the marmoset's frontal eye field. The intermediate subdivision of area 8 (8Ad) has efferent projections to area 7, while the dorsomedial subdivision (8B) has few or no connections with extrastriate cortex. Area 46, located rostrolateral to area 8Av, has substantial connections with the medial extrastriate areas (DM, DA, and area 7) and with MT, while the cortex lateral to 8Av (area 12/45) projects primarily to MT and to the MTc. The rostromedial prefrontal (area 9) and frontopolar (area 10) regions have very few extrastriate projections. Finally, cells in dorsal area 6 (6d) have sparse projections to DM, MT, and the MTc, as well as strong projections to DA and to area 7. These results illuminate aspects of the evolutionary development of the primate frontal cortex, and serve as a basis for further research into cognitive functions using a marmoset model.     

Diverse thalamic projections to the prefrontal cortex in the rhesus monkey.

We studied the sources of thalamic projections to prefrontal areas of nine rhesus monkeys with the aid of retrograde tracers (horseradish peroxidase or fluorescent dyes). Our goal was to determine the proportion of labeled neurons contributing to this projection system by the mediodorsal (MD) nucleus compared to those distributed in other thalamic nuclei, and to investigate the relationship of thalamic projections to specific architectonic areas of the prefrontal cortex. We selected areas for study within both the basoventral (areas 11, 12, and ventral 46) and the mediodorsal (areas 32, 14, 46, and 8) prefrontal sectors. This choice was based on our previous studies, which indicate differences in cortical projections to these two distinct architectonic sectors (Barbas, '88; Barbas and Pandya, '89). In addition, for each sector we included areas with different architectonic profiles, which is also relevant to the connectional patterns of the prefrontal cortices. The results showed that MD included a clear majority (over 80%) of all thalamic neurons directed to some prefrontal cortices (areas 11, 46, and 8); it contributed just over half to some others (areas 12 and 32), and less than a third to area 14. Clusters of neurons directed to basoventral and mediodorsal prefrontal areas were largely segregated within MD: the former were found ventrally, the latter dorsally. However, the most striking findings establish a relationship between thalamic origin and laminar definition of the prefrontal target areas. Most thalamic neurons directed to lateral prefrontal cortices, which are characterized by a high degree of laminar definition (areas 46 and 8), originated in the parvicellular and multiform subdivisions of MD, and only a few were found in other nuclei. In contrast, orbital and medial cortices, which have a low degree of laminar differentiation, were targeted by the magnocellular subdivision of MD and by numerous other limbic thalamic nuclei, including the midline and the anterior. Thus topographic specificity in the origin of thalamic projections increased as the laminar definition of the target area increased. Moreover, the rostrocaudal distribution of labeled neurons in MD and the medial pulvinar also differed depending on the degree of the laminar definition of the prefrontal target areas. The rostral parts of MD and the medial pulvinar projected to the eulaminate lateral prefrontal cortices, whereas their caudal parts projected to orbital and medial limbic cortices. Selective destruction of caudal MD is known to disrupt mnemonic processes in both humans and monkeys, suggesting that this thalamic-limbic prefrontal loop may constitute an important pathway for memory.     

Connections of the marmoset rostrotemporal auditory area: express pathways for analysis of affective content in hearing

The current hierarchical model of primate auditory cortical processing proposes a core of 'primary-like' areas, which is surrounded by secondary (belt) and tertiary (parabelt) regions. The rostrotemporal auditory cortical area (RT) remains the least well characterized of the three proposed core areas, and its functional organization has only recently come under scrutiny. Here we used injections of anterograde and retrograde tracers in the common marmoset ( Callithrix jacchus ) to examine the connectivity of RT and its adjacent areas. As expected from the current model, RT exhibited dense core-like reciprocal connectivity with the ventral division of the medial geniculate body, the rostral core area and the auditory belt, but had weaker connections with the parabelt. However, RT also projected to the ipsilateral rostromedial prefrontal cortex (area 10), the dorsal temporal pole and the ventral caudate nucleus, as well as bilaterally to the lateral nucleus of the amygdala. Thus, RT has connectivity with limbic structures previously believed to connect only with higher-order auditory association cortices, and is probably functionally distinct from the other core areas. While this view is consistent with a proposed role of RT in temporal integration, our results also indicate that RT could provide an anatomical 'shortcut' for processing affective content in auditory information.     

Forebrain connectivity of the prefrontal cortex in the marmoset monkey (Callithrix jacchus): an anterograde and retrograde tract-tracing study

The cortical and subcortical forebrain connections of the marmoset prefrontal cortex (PFC) were examined by injecting the retrograde tracer, choleratoxin, and the anterograde tracer, biotin dextran amine, into four sites within the PFC. Two of the sites, the lateral and orbital regions, had previously been shown to provide functionally dissociable contributions to distinct forms of behavioral flexibility, attentional set-shifting and discrimination reversal learning, respectively. The dysgranular and agranular regions lying on the orbital and medial surfaces of the frontal lobes were most closely connected with limbic structures including cingulate cortex, amygdala, parahippocampal cortex, subiculum, hippocampus, hypothalamus, medial caudate nucleus, and nucleus accumbens as well as the magnocellular division of the mediodorsal nucleus of the thalamus and midline thalamic nuclei, consistent with findings in the rhesus monkey. In contrast, the granular region on the dorsal surface closely resembled area 8Ad in macaques and had connections restricted to posterior parietal cortex primarily associated with visuospatial functions. However, it also had connections with limbic cortex, including retrosplenial and caudal cingulate cortex as well as auditory processing regions in the superior temporal cortex. The granular region on the lateral convexity had the most extensive connections. Based on its architectonics and functionality, it resembled areas 12/45 in macaques. It had connections with high-order visual processing regions in the inferotemporal cortex and posterior parietal cortex, higher-order auditory and polymodal processing regions in the superior temporal cortex. In addition it had extensive connections with limbic regions including the amygdala, parahippocampal cortex, cingulate, and retrosplenial cortex.     

Dual mode of corticothalamic synaptic termination in the mediodorsal nucleus of the rhesus monkey

Electron microscopic autoradiography (EM-ARG) was used to assess the synaptic organization of corticothalamic terminals in the parvicellular division of the mediodorsal thalamic nucleus. Examination of the synaptic organization in unreacted tissue revealed several distinct synaptic types distributed among glomerular and nonglomerular regions of the neuropil. Within glomeruli, three presynaptic terminal classes were found. The majority of profiles (as many as eight to ten per glomerulus) were presynaptic dendrites (PSDs) forming symmetric synaptic contacts with a central dendrite, and occasionally with other PSDs. One or two large terminals densely packed with round vesicles (LR terminals) were also present in each glomerulus. This terminal class made multiple asymmetric contacts with the central dendrite, as well as with many PSDs within the glomerulus. Finally, small terminals with round vesicles (SR terminals) formed asymmetric synaptic junctions with PSDs in some glomeruli. PSDs and SR terminals were also found in the extraglomerular neuropil, although in different proportions than in the glomeruli. In the extraglomerular neuropil SR terminals were the most abundant terminal class and these terminals made synaptic contacts with dendrites of all sizes. PSDs were seen in considerably smaller numbers than in the glomeruli. Finally, the extraglomerular neuropil contained a moderate number of small to medium terminals that formed symmetric synaptic junctions (SF terminals) with cell bodies and dendrites of all sizes. Synaptic profiles related to corticothalamic inputs were identified by injecting the prefrontal cortex of two rhesus monkeys with 3H-leucine and -proline and analyzing the distribution and morphology of radiolabeled terminals. Quantitative analysis of the density of silver grains over different tissue compartments revealed a positive labeling index for two terminal classes: SR and LR terminals. Labeled SR terminals were concentrated in the extraglomerular neuropil and labeled LR terminals were found within glomeruli where they formed synaptic contact with the central dendrite, as well as with presynaptic dendrites of the glomerulus. In contrast to many other thalamic nuclei, cortical input to the mediodorsal nucleus arrives via two distinctive synaptic pathways, one terminating extraglomerularly and the other terminating within the synaptic glomeruli. The dual mode of corticothalamic terminations in the mediodorsal nucleus suggests a more potent and possibly different role for cortical input in the regulation of neuronal activity in this association nucleus than in sensory nuclei of the thalamus.     

Development of non-phosphorylated neurofilament protein expression in neurones of the New World monkey dorsolateral frontal cortex

We studied developmental changes in the expression of non-phosphorylated neurofilament protein (NNF) (a marker of the structural maturation of pyramidal neurones) in the dorsolateral frontal cortex of marmoset monkeys, between embryonic day 130 and adulthood. Our focus was on cortical fields that send strong projections to extrastriate cortex, including the dorsal and ventral subdivisions of area 8A, area 46 and area 6d. For comparison, we also investigated the maturation of prefrontal area 9, which has few or no connections with visual areas. The timing of expression of NNF immunostaining in early life can be described as the result of the interaction of two developmental gradients. First, there is an anteroposterior gradient of maturation in the frontal lobe, whereby neurones in caudal areas express NNF earlier than those in rostral areas. Second, there is a laminar gradient, whereby the first NNF-immunoreactive neurones emerge in layer V, followed by those in progressively more superficial parts of layer III. Following a peak in density of NNF-immunopositive cell numbers in layer V at 2-3 months of age, there is a gradual decline towards adulthood. In contrast, the density of immunopositive cells in layer III continues to increase throughout the first postnatal year in area 6d and until late adolescence (> 1.5 years of age) in prefrontal areas. The present results support the view that the maturation of visual cognitive functions involves relatively late processes linked to structural changes in frontal cortical areas.     

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.     

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.     

Prefrontal cortex afferents to the anterior temporal lobe in the Macaca fascicularis monkey

The anatomical organization of the lateral prefrontal cortex (LPFC) afferents to the anterior part of the temporal lobe (ATL) remains to be clarified. The LPFC has two subdivisions, dorsal (dLPFC) and ventral (vLPFC), which have been linked to cognitive processes. The ATL includes several different cortical areas, namely, the temporal polar cortex and rostral parts of the perirhinal, inferotemporal, and anterior tip of the superior temporal gyrus cortices. Multiple sensory modalities converge in the ATL. All of them (except the rostral inferotemporal and superior temporal gyrus cortices) are components of the medial temporal lobe, which is critical for long‐term memory processing. We studied the LPFC connections with the ATL by placing retrograde tracer injections into the ATL: the temporal polar (n = 3), perirhinal (areas 35 and 36, n = 6), and inferotemporal cortices (area TE, n = 5), plus one additional deposit in the posterior parahippocampal cortex (area TF, n = 1). Anterograde tracer deposits into the dLPFC (A9 and A46, n = 2), the vLPFC (A46v, n = 2), and the orbitofrontal cortex (OF; n = 2) were placed for confirmation of those projections. The results showed that the vLPFC displays a moderate projection to rostral area TE and the dorsomedial portion of the temporal polar cortex; in contrast, the dLPFC connections with the ATL were weak. By comparison, the OFC and medial frontal cortices (MFC) showed dense connectivity with the ATL, namely, A13 with the temporopolar and perirhinal cortices. All areas of the MFC projected to the temporopolar cortex, albeit with a lower intensity. The functional significance of such paucity of LPFC afferents is unknown. J. Comp. Neurol. 523:2570–2598, 2015. © 2015 Wiley Periodicals, Inc.     

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.     

Corticopontine projections from the cingulate cortex in the rhesus monkey

The corticopontine projections of the cingulate cortices were investigated in the rhesus monkey with the use of autoradiography. A well-organized topography of projections was observed with anterior cingulate cortex projecting to the medial part of the pontine gray matter and posterior cingulate cortex projecting to the lateral part. Together these projections form a circle of termination around the periphery of the pontine gray matter.     

Auditory belt and parabelt projections to the prefrontal cortex in the Rhesus monkey

Recent anatomical and electrophysiological studies have expanded our knowledge of the auditory cortical system in primates and have described its organization as a series of concentric circles with a central or primary auditory core, surrounded by a lateral and medial belt of secondary auditory cortex with a tertiary parabelt cortex just lateral to this belt. Because recent studies have shown that rostral and caudal belt and parabelt cortices have distinct patterns of connections and acoustic responsivity, we hypothesized that these divergent auditory regions might have distinct targets in the frontal lobe. We, therefore, placed discrete injections of wheat germ agglutinin-horseradish peroxidase or fluorescent retrograde tracers into the prefrontal cortex of macaque monkeys and analyzed the anterograde and retrograde labeling in the aforementioned auditory areas. Injections that included rostral and orbital prefrontal areas (10, 46 rostral, 12) labeled the rostral belt and parabelt most heavily, whereas injections including the caudal principal sulcus (area 46), periarcuate cortex (area 8a), and ventrolateral prefrontal cortex (area12vl) labeled the caudal belt and parabelt. Projections originating in the parabelt cortex were denser than those arising from the lateral or medial belt cortices in most cases. In addition, the anterior third of the superior temporal gyrus and the dorsal bank of the superior temporal sulcus were also labeled after prefrontal injections, confirming previous studies. The present topographical results suggest that acoustic information diverges into separate streams that target distinct rostral and caudal domains of the prefrontal cortex, which may serve different acoustic functions. J. Comp. Neurol. 403:141–157, 1999. © 1999 Wiley-Liss, Inc.     

Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys

The terminal distribution of thalamic afferents in primate prefrontal cortex has never been examined in any detail. In the present study, WGA-HRP was injected into major subdivisions of the mediodorsal nucleus (MD) in the rhesus monkey in order to determine 1) The areal distribution of MD projections, 2) the layer(s) in which MD afferents terminate, 3) the tangential pattern of the MD axonal terminals, 4) the cells of origin of the reciprocal corticothalamic pathway, and 5) the degree of reciprocity between the corticothalamic and thalamocortical pathways in the different regions of the prefrontal cortex. As expected on the basis of retrograde degeneration and transport studies, injections centered in the magnocellular (MDmc) subnucleus of MD labeled cells and terminals in the ventral and medial prefrontal cortex. Injections involving ventral MDmc labeled the more lateral of these areas (Walker's areas 11 and 12); injections of the dorsal MDmc labeled the ventromedial regions (areas 13 and 14). In contrast, injections involving mainly the lateral, parvicellular (MDpc) moiety labeled cells and terminals in dorsolateral and dorsomedial areas (Walker's 46, 9, and 8B). Area 8A was labeled most prominently when injections included the multiform portion of MD (MDmf) and area 10 had connections with anterior portions of MD. A dorsal-ventral topography for MDpc exists with dorsal MDpc labeling dorsal and dorsomedial prefrontal areas and ventral MDpc labeling dorsolateral prefrontal cortex. Our findings with respect to MD are consistent with a nucleus-to-field organization of its thalamocortical projection system. Outside of the traditional boundaries of prefrontal cortex, lateral MD projections extended to the supplementary motor area (SMA) and the dorsal part of the anterior cingulate (AC) whereas the medial MD projection targeted the ventromedial cingulate cortex and spared SMA. In addition, a few labeled cells and sparse terminals were found in the inferior parietal lobule, the superior temporal sulcus, and the anterior part of the insula after injections that involved the medial part of MD. Labeled terminals were invariably confined to layer IV and adjacent deep layer III. No terminal label was ever observed in layers I, II, superficial III, V, or VI in any part of the cerebral cortex following injections confined to any part of MD.(ABSTRACT TRUNCATED AT 400 WORDS)     

Distribution of neurotensin-containing fibers in the frontal cortex of the macaque monkey.

The distribution of neurotensin-containing fibers was examined in the frontal cortex of the monkey Macaca fuscata using the immunoperoxidase histochemical technique. An extremely dense network of neurotensin-containing fibers was observed in the medial prefrontal regions. The majority of cortical neurotensin fibers was observed in the anterior cingulate cortex (Walker's area 24) and adjacent medial prefrontal regions (areas 6 and 32). In area 24, the fiber density was similar to that in the nucleus accumbens. Immunoreactive fibers were particularly dense in two pyramidal layers (III, V). The medial prefrontal regions, areas 6 and 32, contained a moderate density of immunoreactive fibers. This regional distribution of neurotensin-containing fibers was not observed in other cortical fiber systems that contained substance P, somatostatin, or tyrosine hydroxylase. No neurotensin-containing cell bodies were observed in the frontal cortex. The present study demonstrates that the laminar and regional distributions of neurotensin-containing fibers are unique when compared to those of substance P- or somatostatin-containing fibers, and also distinct from that of catecholaminergic fibers. The distribution of telencephalic neurotensin fibers points to a relationship with limbic structures.     

The origin of projections from the posterior cingulate and retrosplenial cortices to the anterior,medial dorsal and laterodorsal thalamic nuclei of macaque monkeys

Interactions between the posterior cingulate cortex (areas 23 and 31) and the retrosplenial cortex (areas 29 and 30) with the anterior, laterodorsal and dorsal medial thalamic nuclei are thought to support various aspects of cognition, including memory and spatial processing. To detail these interactions better, the present study used retrograde tracers to reveal the origins of the corticothalamic projections in two closely related monkey species (Macaca mulatta, Macaca fascicularis). The medial dorsal thalamic nucleus received only light cortical inputs, which predominantly arose from area 23. Efferents to the anterior medial thalamic nucleus also arose principally from area 23, but these projections proved more numerous than those to the medial dorsal nucleus and also involved additional inputs from areas 29 and 30. The anterior ventral and laterodorsal thalamic nuclei had similar sources of inputs from the posterior cingulate and retrosplenial cortices. For both nuclei, the densest projections arose from areas 29 and 30, with numbers of thalamic inputs often decreasing when going dorsal from area 23a to 23c and to area 31. In all cases, the corticothalamic projections almost always arose from the deepest cortical layer. The different profiles of inputs to the anterior medial and anterior ventral thalamic nuclei reinforce other anatomical and electrophysiological findings suggesting that these adjacent thalamic nuclei serve different, but complementary, functions supporting memory. While the lack of retrosplenial connections singled out the medial dorsal nucleus, the very similar connection patterns shown by the anterior ventral and laterodorsal nuclei point to common roles in cognition.     

Patterns of cortical input to the primary motor area in the marmoset monkey

In primates the primary motor cortex (M1) forms a topographic map of the body, whereby neurons in the medial part of this area control movements involving trunk and hindlimb muscles, those in the intermediate part control movements involving forelimb muscles, and those in the lateral part control movements of facial and other head muscles. This topography is accompanied by changes in cytoarchitectural characteristics, raising the question of whether the anatomical connections also vary between different parts of M1. To address this issue, we compared the patterns of cortical afferents revealed by retrograde tracer injections in different locations within M1 of marmoset monkeys. We found that the entire extent of this area is unified by projections from the dorsocaudal and medial subdivisions of premotor cortex (areas 6DC and 6M), from somatosensory areas 3a, 3b, 1/2, and S2, and from posterior parietal area PE. While cingulate areas projected to all subdivisions, they preferentially targeted the medial part of M1. Conversely, the ventral premotor areas were preferentially connected with the lateral part of M1. Smaller but consistent inputs originated in frontal area 6DR, ventral posterior parietal cortex, the retroinsular cortex, and area TPt. Connections with intraparietal, prefrontal, and temporal areas were very sparse, and variable. Our results demonstrate that M1 is unified by a consistent pattern of major connections, but also shows regional variations in terms of minor inputs. These differences likely reflect requirements for control of voluntary movement involving different body parts. J. Comp. Neurol. 522:811–843, 2014. © 2013 Wiley Periodicals, Inc.     

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.     

Cortical and thalamic projections to cytoarchitectural areas 6Va and 8C of the marmoset monkey: Connectionally distinct subdivisions of the lateral premotor cortex

We studied the afferent connections of two cytoarchitectural subdivisions of the caudolateral frontal cortex, areas 6Va and 8C, in marmoset monkeys. These areas received connections from the same set of thalamic nuclei, including main inputs from the ventral lateral and ventral anterior complexes, but differed in their patterns of corticocortical connections. Areas 8C and 6Va had reciprocal interconnections, and received similar proportions of afferents from premotor areas 6M and 6DC, and from the prefrontal cortex. However, area 8C received stronger inputs from frontal areas that have been implicated in oculomotor functions, whereas area 6Va received stronger projections from the primary motor area. Somatosensory projections to area 6Va were generally stronger than those to area 8C, and originated from several areas; in contrast, only the second somatosensory area (S2) sent major inputs to area 8C. Finally, although both 6Va and 8C received major inputs from the rostral posterior parietal cortex (putative homologs of areas PE, PF, and PFG), area 8C also received a variety of smaller connections from posterior midline, caudal posterior parietal, and extrastriate areas. Statistical analyses revealed that the pattern of connections of area 8C is more akin to that characterizing a premotor area, rather than a prefrontal area. We conclude that cytoarchitectural area 6Va in the marmoset is similar to ventral premotor areas identified in other simian primates, and that area 8C corresponds to a specialized subdivision of the caudal premotor complex where visual information for the guidance of movements is likely to be emphasized. J. Comp. Neurol. 523:1222–1247, 2015. © 2015 Wiley Periodicals, Inc.