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

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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.

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Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe.

C. Cavada, P Goldman-Rakic (1989)

We have examined the circuitry connecting the posterior parietal cortex with the frontal lobe of rhesus monkeys. HRP-WGA and tritiated amino acids were injected into subdivisions 7m, 7a, 7b, and 7ip of the posterior parietal cortex, and anterograde and retrograde label was recorded within the frontal motor and association cortices. Our main finding is that each subdivision of parietal cortex is connected with a unique set of frontal areas. Thus, area 7m, on the medial parietal surface, is interconnected with the dorsal premotor cortex and the supplementary motor area, including the supplementary eye field. Within the prefrontal cortex, area 7m's connections are with the rostral sector of the frontal eye field (FEF), the dorsal bank of the principal sulcus, and the anterior bank of the inferior arcuate sulcus (Walker's area 45). In contrast, area 7a, on the posterior parietal convexity, is not linked with premotor regions but is heavily interconnected with the rostral FEF in the anterior bank of the superior arcuate sulcus, the dorsolateral prefrontal convexity, the rostral orbitofrontal cortex, area 45, and the fundus and adjacent cortex of the dorsal and ventral banks of the principal sulcus. Area 7b, in the anterior part of the posterior parietal lobule, is interconnected with still a different set of frontal areas, which include the ventral premotor cortex and supplementary motor area, area 45, and the external part of the ventral bank of the principal sulcus. The prominent connections of area 7ip, in the posterior bank of the intraparietal sulcus, are with the supplementary eye field and restricted portions of the ventral premotor cortex, with a wide area of the FEF that includes both its rostral and caudal sectors, and with area 45. All frontoparietal connections are reciprocal, and although they are most prominent within a hemisphere, notable interhemispheric connections are also present. These findings provide a basis for a parcellation of the classically considered association cortex of the frontal lobe, particularly the cortex of the principal sulcus, into sectors defined by their specific connections with the posterior parietal subdivisions. Moreover, the present findings, together with those of a companion study (Cavada and Goldman-Rakic: J. Comp. Neurol. this issue) have allowed us to establish multiple linkages between frontal areas and specific limbic and sensory cortices through the posterior parietal cortex. The networks thus defined may form part of the neural substrate of parallel distributed processing in the cerebral cortex.

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Coding of intention in the posterior parietal cortex.

Sérgio Batista, John Andersen, Nicole L. Snyder (1997)

To look at or reach for what we see, spatial information from the visual system must be transformed into a motor plan. The posterior parietal cortex (PPC) is well placed to perform this function, because it lies between visual areas, which encode spatial information, and motor cortical areas. The PPC contains several subdivisions, which are generally conceived as high-order sensory areas. Neurons in area 7a and the lateral intraparietal area fire before and during visually guided saccades. Other neurons in areas 7a and 5 are active before and during visually guided arm movements. These areas are also active during memory tasks in which the animal remembers the location of a target for hundreds of milliseconds before making an eye or arm movement. Such activity could reflect either visual attention or the intention to make movements. This question is difficult to resolve, because even if the animal maintains fixation while directing attention to a peripheral location, the observed neuronal activity could reflect movements that are planned but not executed. To address this, we recorded from the PPC while monkeys planned either reaches or saccades to a single remembered location. We now report that, for most neurons, activity before the movement depended on the type of movement being planned. We conclude that PPC contains signals related to what the animal intends to do.

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Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space.

J. Lynch, V Mountcastle, H. Sakata … (1975)

Experiments were made on the posterior parietal association cortical areas 5 and in 17 hemispheres of 11 monkeys, 6 M. mulatta and 5 M. arctoides. The electrical signs of the activity of single cortical cells were recorded with microelectrodes in waking animals as they carried out certain behavioral acts in response to a series of sensory cues. The behavioral paradigms were one for detection alone, and a second for detection plus projection of the arm to contact a stationary or moving target placed at arm's length. Of the 125 microelectrode penetrations made, 1,451 neurons were identified in terms of the correlation of their activity with the behavioral acts and their sensitivity or lack of it to sensory stimuli delivered passively; 180 were studied quantitatively. The locations of cortical neurons were identified in serial sections; 94 penetrations and 1,058 neurons were located with certainty. About two-thirds of the neurons of area 5 were activated by passive rotation of the limbs at their joints; of these, 82% were related to single, contralateral joints, 10% to two or more contralateral joints, 6% to ipsilateral, and 2% to joints on both sides of the body. A few of the latter were active during complex bodily postures. A large proportion of area 5 neurons were relatively insensitive to passive joint rotations, as compared with similar neurons of the postcentral gyrus, but were driven to high rates of discharge when the same joint was rotated during an active movement of the animal...

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Journal

Journal ID (nlm-ta): eNeuro

Journal ID (iso-abbrev): eNeuro

Journal ID (hwp): eneuro

Journal ID (pmc): eneuro

Journal ID (publisher-id): eNeuro

Title: eNeuro

Publisher: Society for Neuroscience

ISSN (Electronic): 2373-2822

Publication date (Electronic preprint): 30 November 2017

Publication date (Electronic): 8 December 2017

Publication date Collection: Nov-Dec 2017

Volume: 4

Issue: 6

Electronic Location Identifier: ENEURO.0344-17.2017

Affiliations

[1 ]Biomedicine Discovery Institute and Department of Physiology, Monash University , Clayton, Victoria 3800, Australia

[2 ]Australian Research Council, Centre of Excellence for Integrative Brain Function, Monash University Node , Clayton, Victoria 3800, Australia

[3 ]Department of Pharmacy and Biotechnology, University of Bologna , Bologna, 40126, Italy

Author notes

The authors declare no competing financial interests.

Author contributions: S.B., P.F., C.G., and M.G.P.R. designed research; S.B., L.P., T.H., D.I., K.H.W., P.F., K.J.B., and M.G.P.R. performed research; S.B., L.P., T.H., D.I., and M.G.P.R. analyzed data; S.B., C.G., and M.G.P.R. wrote the paper.

Funded by grants from the Australian Research Council (DE120102883, DP140101968, CE140100007), National Health and Medical Research Council (1020839, 1082144), H2020-MSCA-734227–PLATYPUS, MIUR-PRIN, and European Union Fellowship FP7-PEOPLE-2011-IOF 300452 (SB). D.I. received support from the “Erasmus+ International Credit Mobility” fellowship.

Correspondence should be addressed to either of the following: Sophia Bakola or Prof. M.G.P. Rosa, Department of Physiology, Monash University, Clayton VIC 3800, Australia. E-mail: sofia.bakola@ 123456monash.edu or marcello.rosa@ 123456monash.edu .

Author information

Lauretta Passarelli http://orcid.org/0000-0001-5009-2773

Daniele Impieri http://orcid.org/0000-0002-2888-1589

Patrizia Fattori http://orcid.org/0000-0002-0079-3755

Claudio Galletti http://orcid.org/0000-0001-8927-3408

Marcello G. P. Rosa http://orcid.org/0000-0002-6620-6285

Article

Publisher ID: eN-NWR-0344-17

DOI: 10.1523/ENEURO.0344-17.2017

PMC ID: 5779118

PubMed ID: 29379868

SO-VID: e7112031-88b0-414d-993b-2e2db54e95ee

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This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

History

Date received : 8 October 2017

Date revision received : 4 November 2017

Date accepted : 7 November 2017

Page count

Figures: 9, Tables: 3, Equations: 0, References: 139, Pages: 19, Words: 12926

Funding

Funded by: http://doi.org/10.13039/501100000923Australian Research Council (ARC)

Award ID: DE120102883

Award ID: DP140101968

Award ID: CE140100007

Funded by: http://doi.org/10.13039/501100000925Department of Health | National Health and Medical Research Council (NHMRC)

Award ID: 1020839

Award ID: 1082144

Funded by: http://doi.org/10.13039/501100004963EC | Seventh Framework Programme (FP7)

Award ID: FP7-PEOPLE-2011-IOF 300452

Funded by: http://doi.org/10.13039/501100007601EC | Horizon 2020 (EU Framework Programme for Research and Innovation)

Award ID: H2020-MSCA-734227-PLATYPUS

Funded by: http://doi.org/10.13039/501100003407Ministero dell'Istruzione, dell'Università e della Ricerca (MIUR)

Award ID: PRIN

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cover-date November/December 2017

Keywords: connectivity,grasping,parietal,primate,reaching,visuomotor integration

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Keywords: connectivity, grasping, parietal, primate, reaching, visuomotor integration

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

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Most cited references 119

Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe.

Coding of intention in the posterior parietal cortex.

Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space.

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