Parvalbumin as a neurochemical marker of the primate optic radiation.

Parvalbumin (PV) is a calcium-binding protein that labels neuronal cell bodies in the magno and parvocellular layers of the primate lateral geniculate nucleus (LGN). Here we demonstrate that PV immunohistochemistry can also be used to trace the optic radiation (OR) of the marmoset monkey (Callithrix jacchus) from its LGN origin to its destinations in the primary visual cortex (V1), thus providing a high-resolution method for identification of the OR with single axon resolution. The emergence of fibers from LGN, their entire course and even the entry points to V1 were clearly defined in coronal, parasagittal, and horizontal sections of marmoset brain. In all cases, the trajectory revealed by PV staining paralleled that defined by high-resolution diffusion tensor imaging (DTI). We found that V1 was the exclusive target for the PV-containing fibers, with abrupt transitions in staining observed in the white matter at the border with area V2, and no evidence of PV-labeled axons feeding into other visual areas. Changes in the pattern of PV staining in the OR were detected following V1 lesions, demonstrating that this method can be used to assess the progress of retrograde degeneration of geniculocortical projections. These results suggest a technically simple approach to advance our understanding of a major white matter structure, which provides a cellular resolution suitable for the detection of microstructural variations during development, health and disease. Understanding the relationship between PV staining and DTI in non-human primates may also offer clues for improving the specificity and sensitivity of OR tractography for clinical purposes.

Neuronal density and expression of calcium-binding proteins across the layers of the superior colliculus in the common marmoset (Callithrix jacchus).

The superior colliculus (SC) is a layered midbrain structure with functions that include polysensory and sensorimotor integration. Here, we describe the distribution of different immunohistochemically identified classes of neurons in the SC of adult marmoset monkeys (Callithrix jacchus). Neuronal nuclei (NeuN) staining was used to determine the overall neuronal density in the different SC layers. In addition, we studied the distribution of neurons expressing different calcium-binding proteins (calbindin [CB], parvalbumin [PV] and calretinin [CR]). Our results indicate that neuronal density in the SC decreases from superficial to deep layers. Although the neuronal density within the same layer varies little across the mediolateral axis, it tends to be lower at rostral levels, compared to caudal levels. Cells expressing different calcium-binding proteins display differential gradients of density according to depth. Both CB- and CR-expressing neurons show markedly higher densities in the stratum griseum superficiale (SGS), compared to the stratum opticum and intermediate and deep layers. However, CR-expressing neurons are twice as common as CB-expressing neurons outside the SGS. The distribution of PV-expressing cells follows a shallow density gradient from superficial to deep layers. When normalized relative to total neuronal density, the proportion of CR-expressing neurons increases between the superficial and intermediate layers, whereas that of CB-expressing neurons declines toward the deep layers. The proportion of PV-expressing neurons remains constant across layers. Our data provide layer-specific and accurate estimates of neuronal density, which may be important for the generation of biophysical models of how the primate SC transforms sensory inputs into motor signals.

Remodeling of lateral geniculate nucleus projections to extrastriate area MT following long-term lesions of striate cortex.

Here, we report on a previously unknown form of thalamocortical plasticity observed following lesions of the primary visual area (V1) in marmoset monkeys. In primates, lateral geniculate nucleus (LGN) neurons form parallel pathways to the cortex, which are characterized by the expression of different calcium-binding proteins. LGN projections to the middle temporal (MT) area only originate in the koniocellular layers, where many neurons express calbindin. In contrast, projections to V1 also originate in the magnocellular and parvocellular layers, where neurons express parvalbumin but not calbindin. Our results demonstrate that this specificity is disrupted following long-term (1 to 3 y) unilateral V1 lesions, indicating active rearrangement of the geniculocortical circuit. In lesioned animals, retrograde tracing revealed MT-projecting neurons scattered throughout the lesion projection zone (LPZ, the sector of the LGN that underwent retrograde degeneration following a V1 lesion). Many of the MT-projecting neurons had large cell bodies and were located outside the koniocellular layers. Furthermore, we found that a large percentage of magno- and parvocellular neurons expressed calbindin in addition to the expected parvalbumin expression and that this coexpression was present in many of the MT-projecting neurons within the LPZ. These results demonstrate that V1 lesions trigger neurochemical and structural remodeling of the geniculo-extrastriate pathway, leading to the emergence of nonkoniocellular input to MT. This has potential implications for our understanding of the neurobiological bases of the residual visual abilities that survive V1 lesions, including motion perception and blindsight, and reveals targets for rehabilitation strategies to ameliorate the consequences of cortical blindness.

Afferent Connections of Cytoarchitectural Area 6M and Surrounding Cortex in the Marmoset: Putative Homologues of the Supplementary and Pre-supplementary Motor Areas.

Cortical projections to the caudomedial frontal cortex were studied using retrograde tracers in marmosets. We tested the hypothesis that cytoarchitectural area 6M includes homologues of the supplementary and pre-supplementary motor areas (SMA and pre-SMA) of other primates. We found that, irrespective of the injection sites' location within 6M, over half of the labeled neurons were located in motor and premotor areas. Other connections originated in prefrontal area 8b, ventral anterior and posterior cingulate areas, somatosensory areas (3a and 1-2), and areas on the rostral aspect of the dorsal posterior parietal cortex. Although the origin of afferents was similar, injections in rostral 6M received higher percentages of prefrontal afferents, and fewer somatosensory afferents, compared to caudal injections, compatible with differentiation into SMA and pre-SMA. Injections rostral to 6M (area 8b) revealed a very different set of connections, with increased emphasis on prefrontal and posterior cingulate afferents, and fewer parietal afferents. The connections of 6M were also quantitatively different from those of the primary motor cortex, dorsal premotor areas, and cingulate motor area 24d. These results show that the cortical motor control circuit is conserved in simian primates, indicating that marmosets can be valuable models for studying movement planning and control.

Volume reduction without neuronal loss in the primate pulvinar complex following striate cortex lesions.

Lesions in the primary visual cortex (V1) cause extensive retrograde degeneration in the lateral geniculate nucleus, but it remains unclear whether they also trigger any neuronal loss in other subcortical visual centers. The inferior (IPul) and lateral (LPul) pulvinar nuclei have been regarded as part of the pathways that convey visual information to both V1 and extrastriate cortex. Here, we apply stereological analysis techniques to NeuN-stained sections of marmoset brain, in order to investigate whether the volume of these nuclei, and the number of neurons they comprise, change following unilateral long-term V1 lesions. For comparison, the medial pulvinar nucleus (MPul), which has no connections with V1, was also studied. Compared to control animals, animals with lesions incurred either 6 weeks after birth or in adulthood showed significant LPul volume loss following long (> 11 months) survival times. However, no obvious areas of neuronal degeneration were observed. In addition, estimates of neuronal density in lesioned hemispheres were similar to those in the non-lesioned hemispheres of same animals. Our results support the view that, in marked contrast with the geniculocortical projection, the pulvinar pathway is largely spared from the most severe long-term effects of V1 lesions, whether incurred in early postnatal or adult life. This difference can be linked to the more divergent pattern of pulvinar connectivity to the visual cortex, including strong reciprocal connections with extrastriate areas. The results also caution against interpretation of volume loss in brain structures as a marker for neuronal degeneration.

Claustral Input to the Macaque Medial Posterior Parietal Cortex (Superior Parietal Lobule and Adjacent Areas).

The projections from the claustrum to cortical areas within and adjacent to the superior parietal lobule were studied in 10 macaque monkeys, using retrograde tracers, computerized reconstructions, and quantitative methods. In contrast with the classical view that posterior parietal areas receive afferents primarily from the dorsal and posterior regions of the claustrum, we found that these areas receive more extensive projections, including substantial afferents from the anterior and ventral regions of the claustrum. Moreover, our findings uncover a previously unsuspected variability in the precise regions of the claustrum that originate the projections, according to the target areas. For example, areas dominated by somatosensory inputs for control of body movements tend to receive most afferents from the dorsal-posterior claustrum, whereas those which also receive significant visual inputs tend to receive more afferents from the ventral claustrum. In addition, different areas within these broadly defined groups differ in terms of quantitative emphasis in the origin of projections. Overall, these results argue against a simple model whereby adjacency in the cortex determines adjacency in the sectors of claustral origin of projections and indicate that subnetworks defined by commonality of function may be an important factor in defining claustrocortical topography.

Neurochemical changes in the primate lateral geniculate nucleus following lesions of striate cortex in infancy and adulthood: implications for residual vision and blindsight.

Following lesions of the primary visual cortex (V1), the lateral geniculate nucleus (LGN) undergoes substantial cell loss due to retrograde degeneration. However, visually responsive neurons remain in the degenerated sector of LGN, and these have been implicated in mediation of residual visual capacities that remain within the affected sectors of the visual field. Using immunohistochemistry, we compared the neurochemical characteristics of LGN neurons in V1-lesioned marmoset monkeys (Callithrix jacchus) with those of non-lesioned control animals. We found that GABAergic neurons form approximately 6.5% of the neuronal population in the normal LGN, where most of these cells express the calcium-binding protein parvalbumin. Following long-term V1 lesions in adult monkeys, we observed a marked increase (~ sevenfold) in the proportion of GABA-expressing neurons in the degenerated sector of the LGN, indicating that GABAergic cells are less affected by retrograde degeneration in comparison with magno- and parvocellular projection neurons. In addition, following early postnatal V1 lesions and survival into adulthood, we found widespread expression of GABA in putative projection neurons, even outside the degenerated sectors (lesion projection zones). Our findings show that changes in the ratio of GABAergic neurons in LGN need to be taken into account in the interpretation of the mechanisms of visual abilities that survive V1 lesions in primates.

Histology-Based Average Template of the Marmoset Cortex With Probabilistic Localization of Cytoarchitectural Areas.

The rapid adoption of marmosets in neuroscience has created a demand for three dimensional (3D) atlases of the brain of this species to facilitate data integration in a common reference space. We report on a new open access template of the marmoset cortex (the Nencki-Monash, or NM template), representing a morphological average of 20 brains of young adult individuals, obtained by 3D reconstructions generated from Nissl-stained serial sections. The method used to generate the template takes into account morphological features of the individual brains, as well as the borders of clearly defined cytoarchitectural areas. This has resulted in a resource which allows direct estimates of the most likely coordinates of each cortical area, as well as quantification of the margins of error involved in assigning voxels to areas, and preserves quantitative information about the laminar structure of the cortex. We provide spatial transformations between the NM and other available marmoset brain templates, thus enabling integration with magnetic resonance imaging (MRI) and tracer-based connectivity data. The NM template combines some of the main advantages of histology-based atlases (e.g. information about the cytoarchitectural structure) with features more commonly associated with MRI-based templates (isotropic nature of the dataset, and probabilistic analyses). The underlying workflow may be found useful in the future development of 3D brain atlases that incorporate information about the variability of areas in species for which it may be impractical to ensure homogeneity of the sample in terms of age, sex and genetic background.

Open access resource for cellular-resolution analyses of corticocortical connectivity in the marmoset monkey.

Understanding the principles of neuronal connectivity requires tools for efficient quantification and visualization of large datasets. The primate cortex is particularly challenging due to its complex mosaic of areas, which in many cases lack clear boundaries. Here, we introduce a resource that allows exploration of results of 143 retrograde tracer injections in the marmoset neocortex. Data obtained in different animals are registered to a common stereotaxic space using an algorithm guided by expert delineation of histological borders, allowing accurate assignment of connections to areas despite interindividual variability. The resource incorporates tools for analyses relative to cytoarchitectural areas, including statistical properties such as the fraction of labeled neurons and the percentage of supragranular neurons. It also provides purely spatial (parcellation-free) data, based on the stereotaxic coordinates of 2 million labeled neurons. This resource helps bridge the gap between high-density cellular connectivity studies in rodents and imaging-based analyses of human brains.

Thalamic afferents emphasize the different functions of macaque precuneate areas.

We studied the thalamic afferents to cortical areas in the precuneus using injections of retrograde fluorescent neuronal tracers in four male macaques (Macaca fascicularis). Six injections were within the limits of cytoarchitectural area PGm, one in area 31 and one in area PEci. Precuneate areas shared strong input from the posterior thalamus (lateral posterior nucleus and pulvinar complex) and moderate input from the medial, lateral, and intralaminar thalamic regions. Area PGm received strong connections from the subdivisions of the pulvinar linked to association and visual function (the medial and lateral nuclei), whereas areas 31 and PEci received afferents from the oral division of the pulvinar. All three cytoarchitectural areas also received input from subdivisions of the lateral thalamus linked to motor function (ventral lateral and ventral anterior nuclei), with area PEci receiving additional input from a subdivision linked to somatosensory function (ventral posterior lateral nucleus). Finally, only PGm received substantial limbic association afferents, mainly via the lateral dorsal nucleus. These results indicate that area PGm integrates information from visual association, motor and limbic regions of the thalamus, in line with a hypothesized role in spatial cognition, including navigation. By comparison, dorsal precuneate areas (31 and PEci) are more involved in sensorimotor functions, being akin to adjacent areas of the dorsal parietal cortex.

Internal Subdivisions of the Marmoset Claustrum Complex: Identification by Myeloarchitectural Features and High Field Strength Imaging.

There has been a surge of interest in the structure and function of the mammalian claustrum in recent years. However, most anatomical and physiological studies treat the claustrum as a relatively homogenous structure. Relatively little attention has been directed toward possible compartmentalization of the claustrum complex into anatomical subdivisions, and how this compartmentalization is reflected in claustrum connections with other brain structures. In this study, we examined the cyto- and myelo-architecture of the claustrum of the common marmoset (Callithrix jacchus), to determine whether the claustrum contains internal anatomical structures or compartments, which could facilitate studies focused on understanding its role in brain function. NeuN, Nissl, calbindin, parvalbumin, and myelin-stained sections from eight adult marmosets were studied using light microscopy and serial reconstruction to identify potential internal compartments. Ultra high resolution (9.4T) post-mortem magnetic resonance imaging was employed to identify tractographic differences between identified claustrum subcompartments by diffusion-weighted tractography. Our results indicate that the classically defined marmoset claustrum includes at least two major subdivisions, which correspond to the dorsal endopiriform and insular claustrum nuclei, as described in other species, and that the dorsal endopiriform nucleus (DEnD) contains architecturally distinct compartments. Furthermore, the dorsal subdivision of the DEnD is tractographically distinguishable from the insular claustrum with respect to cortical connections.

Topographic Organization of the 'Third-Tier' Dorsomedial Visual Cortex in the Macaque.

The boundaries of the visual areas located anterior to V2 in the dorsomedial region of the macaque cortex remain contentious. This region is usually conceptualized as including two functional subdivisions: the dorsal component of area V3 (V3d) laterally and another area named the parietooccipital area (PO) or V6 medially. However, the nature of the putative border between V3d and PO/V6 has remained undefined. We recorded the receptive fields of multiunit clusters in male macaques and reconstructed the locations of recording sites using histological sections and computer-generated maps. Immediately adjacent to dorsomedial V2, we observed a representation of the lower contralateral quadrant that represented the vertical meridian at its rostral border. This region formed a simple eccentricity gradient from ∼<5° in the annectant gyrus to >60° in the parietooccipital medial sulcus. There was no topographic reversal where one would expect to find the border between V3d and PO/V6. Rather, near the midline, this lower quadrant map continued directly into a representation of the peripheral upper visual field without an intervening lower quadrant representation. Therefore, cortex previously assigned to the medial part of V3d and to PO/V6 forms a single map that includes parts of both quadrants. Together with previous observations that V3d and PO/V6 are densely myelinated relative to adjacent cortex and share similar input from V1, these results suggest that they are parts of a single area (for which we suggest the designation V6), which is distinct from the one forming the ventral component of the third-tier complex.SIGNIFICANCE STATEMENT The primate visual cortex has a large number of areas. Knowing the extent of each visual area and how they can be distinguished from each other is essential for the interpretation of experiments aimed at understanding visual processing. Currently, there are conflicting models of the organization of the dorsomedial visual cortex rostral to area V2 (one of the earliest stages of cortical processing of vision). By conducting large-scale electrophysiological recordings, we found that what were originally thought to be distinct areas in this region (dorsal V3 and the parietooccipital area PO/V6), together form a single map of the visual field. This will help to guide future functional studies and the interpretation of the outcomes of lesions involving the dorsal visual cortex.

Neuronal Distribution Across the Cerebral Cortex of the Marmoset Monkey (Callithrix jacchus).

Using stereological analysis of NeuN-stained sections, we investigated neuronal density and number of neurons per column throughout the marmoset cortex. Estimates of mean neuronal density encompassed a greater than 3-fold range, from >150 000 neurons/mm3 in the primary visual cortex to ~50 000 neurons/mm3 in the piriform complex. There was a trend for density to decrease from posterior to anterior cortex, but also local gradients, which resulted in a complex pattern; for example, in frontal, auditory, and somatosensory cortex neuronal density tended to increase towards anterior areas. Anterior cingulate, motor, premotor, insular, and ventral temporal areas were characterized by relatively low neuronal densities. Analysis across the depth of the cortex revealed greater laminar variation of neuronal density in occipital, parietal, and inferior temporal areas, in comparison with other regions. Moreover, differences between areas were more pronounced in the supragranular layers than in infragranular layers. Calculations of the number of neurons per unit column revealed a pattern that was distinct from that of neuronal density, including local peaks in the posterior parietal, superior temporal, precuneate, frontopolar, and temporopolar regions. These results suggest that neuronal distribution in adult cortex result from a complex interaction of developmental/ evolutionary determinants and functional requirements.

Unidirectional monosynaptic connections from auditory areas to the primary visual cortex in the marmoset monkey.

Until the late twentieth century, it was believed that different sensory modalities were processed by largely independent pathways in the primate cortex, with cross-modal integration only occurring in specialized polysensory areas. This model was challenged by the finding that the peripheral representation of the primary visual cortex (V1) receives monosynaptic connections from areas of the auditory cortex in the macaque. However, auditory projections to V1 have not been reported in other primates. We investigated the existence of direct interconnections between V1 and auditory areas in the marmoset, a New World monkey. Labelled neurons in auditory cortex were observed following 4 out of 10 retrograde tracer injections involving V1. These projections to V1 originated in the caudal subdivisions of auditory cortex (primary auditory cortex, caudal belt and parabelt areas), and targeted parts of V1 that represent parafoveal and peripheral vision. Injections near the representation of the vertical meridian of the visual field labelled few or no cells in auditory cortex. We also placed 8 retrograde tracer injections involving core, belt and parabelt auditory areas, none of which revealed direct projections from V1. These results confirm the existence of a direct, nonreciprocal projection from auditory areas to V1 in a different primate species, which has evolved separately from the macaque for over 30 million years. The essential similarity of these observations between marmoset and macaque indicate that early-stage audiovisual integration is a shared characteristic of primate sensory processing.

Robust Visual Responses and Normal Retinotopy in Primate Lateral Geniculate Nucleus following Long-term Lesions of Striate Cortex.

Lesions of striate cortex (V1) trigger massive retrograde degeneration of neurons in the LGN. In primates, these lesions also lead to scotomas, within which conscious vision is abolished. Mediation of residual visual capacity within these regions (blindsight) has been traditionally attributed to an indirect visual pathway to the extrastriate cortex, which involves the superior colliculus and pulvinar complex. However, recent studies have suggested that preservation of the LGN is critical for behavioral evidence of blindsight, raising the question of what type of visual information is channeled by remaining neurons in this structure. A possible contribution of LGN neurons to blindsight is predicated on two conditions: that the neurons that survive degeneration remain visually responsive, and that their receptive fields continue to represent the region of the visual field inside the scotoma. We tested these conditions in male and female marmoset monkeys (Callithrix jacchus) with partial V1 lesions at three developmental stages (early postnatal life, young adulthood, old age), followed by long recovery periods. In all cases, recordings from the degenerated LGN revealed neurons with well-formed receptive fields throughout the scotoma. The responses were consistent and robust, and followed the expected eye dominance and retinotopy observed in the normal LGN. The responses had short latencies and preceded those of neurons recorded in the extrastriate middle temporal area. These findings suggest that the pathway that links LGN neurons to the extrastriate cortex is physiologically viable and can support residual vision in animals with V1 lesions incurred at various ages.SIGNIFICANCE STATEMENT Patients with a lesion of the primary visual cortex (V1) can retain certain visually mediated behaviors, particularly if the lesion occurs early in life. This phenomenon ("blindsight") not only sheds light on the nature of consciousness, but also has implications for studies of brain circuitry, development, and plasticity. However, the pathways that mediate blindsight have been the subject of debate. Recent studies suggest that projections from the LGN might be critical, but this finding is puzzling given that the lesions causes severe cell death in the LGN. Here we demonstrate in monkeys that the surviving LGN neurons retain a remarkable level of visual function and could therefore be the source of the visual information that supports blindsight.

Uniformity and Diversity of Cortical Projections to Precuneate Areas in the Macaque Monkey: What Defines Area PGm?

We report on the corticocortical connections of areas on the mesial surface of the macaque posterior parietal cortex, based on 10 retrograde tracer injections targeting different parts of the precuneate gyrus. Analysis of afferent connections supported the existence of two areas: PGm (also known as 7 m) and area 31. Both areas received major afferents from the V6A complex and from the external subdivision of area 23, but they differed in most other aspects. Area 31 showed greater emphasis on connections with premotor and parietal sensorimotor areas, whereas PGm received a greater proportion of its afferents from visuomotor structures involved in spatial cognition (including the lateral intraparietal cortex, inferior parietal lobule, and the putative visual areas in the ventral part of the precuneus). Medially, the anterior cingulate cortex (area 24) preferentially targeted area 31, whereas retrosplenial areas preferentially targeted PGm. These results indicate that earlier views on the connections of PGm were based on tracer injections that included parts of adjacent areas (including area 31), and prompt a reassessment of the limits of PGm. Our findings are compatible with a primary role of PGm in visuospatial cognition (including navigation), while supporting a role for area 31 in sensorimotor planning and coordination.

Neuronal degeneration in the dorsal lateral geniculate nucleus following lesions of primary visual cortex: comparison of young adult and geriatric marmoset monkeys.

Neuronal loss in the lateral geniculate nucleus (LGN) is a consequence of lesions of the primary visual cortex (V1). Despite the importance of this phenomenon in understanding the residual capacities of the primate visual system following V1 damage, few quantitative studies are available, and the effect of age at the time of lesion remains unknown. We compared the volume, neuronal number, and neuronal density in the LGN, 6-21 months after unilateral V1 lesions in marmoset monkeys. Stereological sampling techniques and neuronal nuclei (NeuN) staining were used to assess the effects of similar-sized lesions in adult (2-4 years) and geriatric (10-14 years) animals. We found that lesions involving the opercular and caudal calcarine parts of V1 caused robust loss of neurons in topographically corresponding regions of the ipsilateral LGN (lesion projection zones), concomitant with a substantial reduction in the volume of this nucleus. Neuronal density was markedly reduced in the lesion projection zones, relative to the corresponding regions of the contralateral LGN, or the LGN in non-lesioned animals. Moreover, the percentage decrease in neuronal density within the lesion projection zones was significantly greater in the geriatric group, compared with the adult groups. The volume and neuronal density in the contralateral LGN of lesioned adult and geriatric marmosets were similar to those in non-lesioned animals. These results show that the primate LGN becomes more vulnerable to degeneration with advancing age. However, even in geriatric primates there is a population of LGN neurons which survives degeneration, and which could play a role in blindsight.

Cortical Afferents and Myeloarchitecture Distinguish the Medial Intraparietal Area (MIP) from Neighboring Subdivisions of the Macaque Cortex.

The parietal reach region (PRR) in the medial bank of the macaque intraparietal sulcus has been a subject of considerable interest in research aimed at the development of brain-controlled prosthetic arms, but its anatomical organization remains poorly characterized. We examined the anatomical organization of the putative PRR territory based on myeloarchitecture and retrograde tracer injections. We found that the medial bank includes three areas: an extension of the dorsal subdivision of V6A (V6Ad), the medial intraparietal area (MIP), and a subdivision of area PE (PEip). Analysis of corticocortical connections revealed that both V6Ad and MIP receive inputs from visual area V6; the ventral subdivision of V6A (V6Av); medial (PGm, 31), superior (PEc), and inferior (PFG/PF) parietal association areas; and intraparietal areas AIP and VIP. They also receive long-range projections from the superior temporal sulcus (MST, TPO), cingulate area 23, and the dorsocaudal (area F2) and ventral (areas F4/F5) premotor areas. In comparison with V6Ad, MIP receives denser input from somatosensory areas, the primary motor cortex, and the medial motor fields, as well as from visual cortex in the ventral precuneate cortex and frontal regions associated with oculomotor guidance. Unlike MIP, V6Ad receives stronger visual input, from the caudal inferior parietal cortex (PG/Opt) and V6Av, whereas PEip shows marked emphasis on anterior parietal, primary motor, and ventral premotor connections. These anatomical results suggest that MIP and V6A have complementary roles in sensorimotor behavior, with MIP more directly involved in movement planning and execution in comparison with V6A.

Visually evoked responses in extrastriate area MT after lesions of striate cortex in early life.

Lesions of striate cortex [primary visual cortex (V1)] in adult primates result in blindness. In contrast, V1 lesions in neonates typically allow much greater preservation of vision, including, in many human patients, conscious perception. It is presently unknown how this marked functional difference is related to physiological changes in cortical areas that are spared by the lesions. Here we report a study of the middle temporal area (MT) of adult marmoset monkeys that received unilateral V1 lesions within 6 weeks of birth. In contrast with observations after similar lesions in adult monkeys, we found that virtually all neurons in the region of MT that was deprived of V1 inputs showed robust responses to visual stimulation. These responses were very similar to those recorded in neurons with receptive fields outside the lesion projection zones in terms of firing rate, signal-to-noise ratio, and latency. In addition, the normal retinotopic organization of MT was maintained. Nonetheless, we found evidence of a very specific functional deficit: direction selectivity, a key physiological characteristic of MT that is known to be preserved in many cells after adult V1 lesions, was absent. These results demonstrate that lesion-induced reorganization of afferent pathways is sufficient to develop robust visual function in primate extrastriate cortex, highlighting a likely mechanism for the sparing of vision after neonatal V1 lesions. However, they also suggest that interactions with V1 in early postnatal life are critical for establishing stimulus selectivity in MT.

Contrasting patterns of cortical input to architectural subdivisions of the area 8 complex: a retrograde tracing study in marmoset monkeys.

Contemporary studies recognize 3 distinct cytoarchitectural and functional areas within the Brodmann area 8 complex, in the caudal prefrontal cortex: 8b, 8aD, and 8aV. Here, we report on the quantitative characteristics of the cortical projections to these areas, using injections of fluorescent tracers in marmoset monkeys. Area 8b was distinct from both 8aD and 8aV due to its connections with medial prefrontal, anterior cingulate, superior temporal polysensory, and ventral midline/retrosplenial areas. In contrast, areas 8aD and 8aV received the bulk of the projections from posterior parietal cortex and dorsal midline areas. In the frontal lobe, area 8aV received projections primarily from ventrolateral areas, while both 8aD and 8b received dense inputs from areas on the dorsolateral surface. Whereas area 8aD received the most significant auditory projections, these were relatively sparse, in comparison with those previously reported in macaques. Finally, area 8aV was distinct from both 8aD and 8b by virtue of its widespread input from the extrastriate visual areas. These results are compatible with a homologous organization of the prefrontal cortex in New and Old World monkeys, and suggest significant parallels between the present pathways, revealed by tract-tracing, and networks revealed by functional connectivity analysis in Old World monkeys and humans.