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.

Receptor-driven, multimodal mapping of cortical areas in the macaque monkey intraparietal sulcus.

The intraparietal sulcus (IPS) is structurally and functionally heterogeneous. We performed a quantitative cyto-/myelo- and receptor architectonical analysis to provide a multimodal map of the macaque IPS. We identified 17 cortical areas, including novel areas PEipe, PEipi (external and internal subdivisions of PEip), and MIPd. Multivariate analyses of receptor densities resulted in a grouping of areas based on the degree of (dis)similarity of their receptor architecture: a cluster encompassing areas located in the posterior portion of the IPS and associated mainly with the processing of visual information, a cluster including areas found in the anterior portion of the IPS and involved in sensorimotor processing, and an 'intermediate' cluster of multimodal association areas. Thus, differences in cyto-/myelo- and receptor architecture segregate the cortical ribbon within the IPS, and receptor fingerprints provide novel insights into the relationship between the structural and functional segregation of this brain region in the macaque monkey.

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.

Receptor density pattern confirms and enhances the anatomic-functional features of the macaque superior parietal lobule areas.

The macaque monkey superior parietal lobule (SPL) is part of a neuronal network involved in the integration of information from visual and somatosensory cortical areas for execution of reaching and grasping movements. We applied quantitative in vitro receptor autoradiography to analyse the distribution patterns of 15 different receptors for glutamate, GABA, acetylcholine, serotonin, dopamine, and adenosine in the SPL of three adult male Macaca fascicularis monkeys. For each area, mean (averaged over all cortical layers) receptor densities were visualized as a receptor fingerprint of that area. Multivariate analyses were conducted to detect clusters of areas according to the degree of (dis)similarity of their receptor organization. Differences in regional and laminar receptor distributions confirm the location and extent of areas V6, V6Av, V6Ad, PEc, PEci, and PGm as found in cytoarchitectonic and functional studies, but also enable the definition of three subdivisions within area PE. Receptor densities are higher in supra- than in infragranular layers, with the exception of kainate, M2, and adenosine receptors. Glutamate and GABAergic receptors are the most expressed in all areas analysed. Hierarchical cluster analyses demonstrate that SPL areas are organized in two groups, an organization that corresponds to the visual or sensory-motor characteristics of those areas. Finally, based on present results and in the framework of our current understanding of the structural and functional organization of the primate SPL, we propose a novel pattern of homologies between human and macaque SPL areas.

Thalamo-cortical projections to the macaque superior parietal lobule areas PEc and PE.

The exposed surface of the superior parietal lobule in macaque brain contains two architectonically defined areas named PEc and PE. The aim of the present study is the characterization of thalamic afferents of these two areas. For this purpose, retrograde neuronal tracers were injected, or placed in crystal form, in areas PEc and PE. We found that the two areas show a similar pattern of thalamic inputs, mainly originating from Lateral Posterior (LP), Pulvinar (Pul), Ventral Posterior Lateral (VPL), and Ventral Lateral (VL) nuclei, all structures known to be involved in visual, somatosensory, and/or sensorimotor processing. Minor afferents were observed from the Centromedian/Parafascicular complex (CM/PF), Central Lateral (CL), Ventral Anterior (VA), and Medial Dorsal (MD) nuclei. LP and VL were more strongly connected to PEc than to PE, while the other main thalamic inputs to the two areas showed slight differences in strength. The part of the Pul mostly connected with areas PEc and PE was the Medial Pul. No labeled cells were found in the retinotopically organized Lateral and Inferior Pul. In the somatotopically organized VPL and VL nuclei, labeled neurons were mainly found in regions likely to correspond to the trunk and limb representations (in particular the legs). These findings are in line with the sensory-motor nature of areas PEc and PE, and with their putative functional roles, being them suggested to be involved in the preparation and control of limb interaction with the environment, and in locomotion.

Claustral afferents of superior parietal areas PEc and PE in the macaque.

The exposed surface of the primate superior parietal cortex includes two cytoarchitectonically defined areas, the PEc and PE. In the present study we describe the distribution of neurons projecting from the claustrum to these areas. Retrograde neuronal tracers were injected by direct visualization of regions of interest, and the location of injection sites was reconstructed relative to cytoarchitectural borders. For comparison, the patterns of claustral label that resulted from injections involving neighboring cytoarchitectonic areas were analyzed. We found that the claustral territories sending projections to areas PE and PEc partially overlapped zones previously shown to form projections to the posterior parietal, somatosensory, visual, and motor cortex. The projection zones to the PE and PEc overlapped extensively, and consisted of multiple patches separated by label-free zones. Most of the labeled neurons were located in the posterior-ventral part of the claustrum. Area PE received additional inputs from a posterior-dorsal part of the claustrum, which has been previously reported to project to the somatosensory cortex, while the PEc receives additional input from an anterior-ventral region of the claustrum, which has been reported to project to the visual association cortex. These observations reflect the known functional properties of the PE and PEc, with the former containing neurons that are predominantly involved in somatosensory processing, and the latter including both somatosensory and visual neurons. The present results suggest that the claustrum projections may help coordinate the activity of an extensive neural circuit involved in sensory and motor processing for movement execution. J. Comp. Neurol. 525:1475-1488, 2017. © 2016 Wiley Periodicals, Inc.

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.