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

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Abstract

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.

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Most cited references 78

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Segregation of form, color, movement, and depth: anatomy, physiology, and perception

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Anatomical and physiological observations in monkeys indicate that the primate visual system consists of several separate and independent subdivisions that analyze different aspects of the same retinal image: cells in cortical visual areas 1 and 2 and higher visual areas are segregated into three interdigitating subdivisions that differ in their selectivity for color, stereopsis, movement, and orientation. The pathways selective for form and color seem to be derived mainly from the parvocellular geniculate subdivisions, the depth- and movement-selective components from the magnocellular. At lower levels, in the retina and in the geniculate, cells in these two subdivisions differ in their color selectivity, contrast sensitivity, temporal properties, and spatial resolution. These major differences in the properties of cells at lower levels in each of the subdivisions led to the prediction that different visual functions, such as color, depth, movement, and form perception, should exhibit corresponding differences. Human perceptual experiments are remarkably consistent with these predictions. Moreover, perceptual experiments can be designed to ask which subdivisions of the system are responsible for particular visual abilities, such as figure/ground discrimination or perception of depth from perspective or relative movement--functions that might be difficult to deduce from single-cell response properties.

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The space around us is represented not once but many times in parietal cortex. These multiple representations encode locations and objects of interest in several egocentric reference frames. Stimulus representations are transformed from the coordinates of receptor surfaces, such as the retina or the cochlea, into the coordinates of effectors, such as the eye, head, or hand. The transformation is accomplished by dynamic updating of spatial representations in conjunction with voluntary movements. This direct sensory-to-motor coordinate transformation obviates the need for a single representation of space in environmental coordinates. In addition to representing object locations in motoric coordinates, parietal neurons exhibit strong modulation by attention. Both top-down and bottom-up mechanisms of attention contribute to the enhancement of visual responses. The saliance of a stimulus is the primary factor in determining the neural response to it. Although parietal neurons represent objects in motor coordinates, visual responses are independent of the intention to perform specific motor acts.

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Delays in sensorimotor loops have led to the proposal that reaching movements are primarily under pre-programmed control and that sensory feedback loops exert an influence only at the very end of a trajectory. The present review challenges this view. Although behavioral data suggest that a motor plan is assembled prior to the onset of movement, more recent studies have indicated that this initial plan does not unfold unaltered, but is updated continuously by internal feedback loops. These loops rely on a forward model that integrates the sensory inflow and motor outflow to evaluate the consequence of the motor commands sent to a limb, such as the arm. In such a model, the probable position and velocity of an effector can be estimated with negligible delays and even predicted in advance, thus making feedback strategies possible for fast reaching movements. The parietal lobe and cerebellum appear to play a crucial role in this process. The ability of the motor system to estimate the future state of the limb might be an evolutionary substrate for mental operations that require an estimate of sequelae in the immediate future.

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Author and article information

Contributors

Nicola Palomero-Gallagher:

ORCID: https://orcid.org/0000-0003-4463-8578

Timothy E Behrens: Role: Reviewing Editor

Timothy E Behrens: Role: Senior Editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 02 July 2020

Publication date Collection: 2020

Volume: 9

Electronic Location Identifier: e55979

Affiliations

[1 ]Institute of Neuroscience and Medicine (INM-1), Research Centre Jülich JülichGermany

[2 ]Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty AachenGermany

[3 ]C. & O. Vogt Institute for Brain Research, Heinrich-Heine-University DüsseldorfGermany

[4 ]JARA-BRAIN, Jülich-Aachen Research Alliance JülichGermany

University of Oxford United Kingdom

Laboratory for Neuro-and Psychophysiology Belgium

Author information

Meiqi Niu https://orcid.org/0000-0001-7937-5814

Nicola Palomero-Gallagher https://orcid.org/0000-0003-4463-8578

Article

Publisher ID: 55979

DOI: 10.7554/eLife.55979

PMC ID: 7365665

PubMed ID: 32613942

SO-VID: 6200b5f1-f173-4a3e-8239-dcda1956e258

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This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

History

Date received : 12 February 2020

Date accepted : 01 July 2020

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100000780, European Commission;

Award ID: 785907

Award Recipient : Nicola Palomero-Gallagher Karl Zilles

Funded by: FundRef http://dx.doi.org/10.13039/501100002347, Bundesministerium für Bildung und Forschung;

Award ID: 01GQ1902

Award Recipient : Nicola Palomero-Gallagher

Funded by: FundRef http://dx.doi.org/10.13039/501100000780, European Commission;

Award ID: 945539

Award Recipient : Nicola Palomero-Gallagher Karl Zilles

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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Author impact statement The macaque monkey intraparietal sulcus encompasses 17 cyto- and receptorarchitectonically distinct areas, which can be grouped into three clusters based on (dis)similarities of their molecular structure.

ScienceOpen disciplines: Life sciences

Keywords: intraparietal sulcus,transmitter receptors,cytoarchitecture,myeloarchitecture,multimodal map,rhesus macaque

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ScienceOpen disciplines: Life sciences

Keywords: intraparietal sulcus, transmitter receptors, cytoarchitecture, myeloarchitecture, multimodal map, rhesus macaque

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

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Most cited references 78

Segregation of form, color, movement, and depth: anatomy, physiology, and perception

Space and attention in parietal cortex.

Forward modeling allows feedback control for fast reaching movements.

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