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Open Access 01-11-2020 | Original Article

Wide-field retinotopy reveals a new visuotopic cluster in macaque posterior parietal cortex

Authors: Samy Rima, Benoit R. Cottereau, Yseut Héjja-Brichard, Yves Trotter, Jean-Baptiste Durand

Published in: Brain Structure and Function | Issue 8/2020

Abstract

We investigated the visuotopic organization of macaque posterior parietal cortex (PPC) by combining functional imaging (fMRI) and wide-field retinotopic mapping in two macaque monkeys. Whole brain blood-oxygen-level-dependent (BOLD) signal was recorded while monkeys maintained central fixation during the presentation of large rotating wedges and expending/contracting annulus of a “shaking” fruit basket, designed to maximize the recruitment of PPC neurons. Results of the surface-based population receptive field (pRF) analysis reveal a new cluster of four visuotopic areas at the confluence of the parieto-occipital and intra-parietal sulci, in a location previously defined histologically and anatomically as the posterior intra-parietal (PIP) region. This PIP cluster groups together two recently described areas (CIP1/2) laterally and two newly identified ones (PIP1/2) medially, whose foveal representations merge in the fundus of the intra-parietal sulcus. The cluster shares borders with other visuotopic areas: V3d posteriorly, V3A/DP laterally, V6/V6A medially and LIP anteriorly. Together, these results show that monkey PPC is endowed with a dense set of visuotopic areas, as its human counterpart. The fact that fMRI and wide-field stimulation allows a functional parsing of monkey PPC offers a new framework for studying functional homologies with human PPC.

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Alvarez I, de Haas B, Clark CA, Rees G, Schwarzkopf DS (2015) Comparing different stimulus configurations for population receptive field mapping in human fMRI. Front Hum Neurosci 9:96PubMedPubMedCentral

Andersen RA, Asanuma C, Essick G, Siegel RM (1990) Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule. J Comp Neurol 296:65–113PubMed

Arcaro MJ, Pinsk MA, Li X, Kastner S (2011) Visuotopic organization of macaque posterior parietal cortex: a functional magnetic resonance imaging study. J Neurosci 31:2064–2078PubMedPubMedCentral

Ben Hamed S, Duhamel JR, Bremmer F, Graf W (2001) Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis. Exp Brain Res 140:127–144PubMed

Blatt GJ, Andersen RA, Stoner GR (1990) Visual receptive field organization and cortico-cortical connections of the lateral intraparietal area (area LIP) in the macaque. J Comp Neurol 299:421–445PubMed

Brewer AA, Barton B (2012) Visual field map organization in human visual cortex. Vis Cortex Curr Status Perspect. https://doi.org/10.5772/51914CrossRef

Buneo CA, Andersen RA (2006) The posterior parietal cortex: sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia 44:2594–2606PubMed

Colby CL, Gattass R, Olson CR, Gross CG (1988) Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study. J Comp Neurol 269:392–413PubMed

Cottereau BR, Smith AT, Rima S, Fize D, Héjja-Brichard Y, Renaud L, Lejards C, Vayssière N, Trotter Y, Durand JB (2017) Processing of egomotion-consistent optic flow in the rhesus macaque cortex. Cereb Cortex 27:330–343PubMedPubMedCentral

Dumoulin SO, Wandell BA (2008) Population receptive field estimates in human visual cortex. Neuroimage 39:647–660PubMed

Durand JB, Nelissen K, Joly O, Wardak C, Todd JT, Norman JF, Janssen P, Vanduffel W, Orban GA (2007) Anterior regions of monkey parietal cortex process visual 3d shape. Neuron 55:493–505PubMedPubMedCentral

Engel SA, Glover GH, Wandell BA (1997) Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb Cortex 7:181–192

Freedman DJ, Ibos G (2018) An integrative framework for sensory, motor, and cognitive functions of the posterior parietal cortex. Neuron 97:1219–1234PubMedPubMedCentral

Galletti C, Fattori P, Gamberini M, Kutz DF (1999a) The cortical visual area V6: brain location and visual topography. Eur J Neurosci 11:3922–3936PubMed

Galletti C, Fattori P, Kutz DF, Gamberini M (1999b) Brain location and visual topography of cortical area V6A in the macaque monkey. Eur J Neurosci 11:575–582PubMed

Gamberini M, Fattori P, Galletti C (2015) The medial parietal occipital areas in the macaque monkey. Vis Neurosci 32:E013PubMed

Gattass R, Sousa AP, Gross CG (1988) Visuotopic organization and extent of V3 and V4 of the macaque. J Neurosci 8:1831–1845PubMedPubMedCentral

Georgieva S, Peeters R, Kolster H, Todd JT, Orban GA (2009) The processing of three-dimensional shape from disparity in the human brain. J Neurosci 29:727–742PubMedPubMedCentral

Hadjidimitrakis K, Bakola S, Chaplin TA, Yu H-H, Alanazi O, Chan JM, Worthy KH, Rosa MGP (2019a) Topographic organization of the “third tier” dorsomedial visual cortex in the macaque. J Neurosci 39(27):5311–5325PubMedPubMedCentral

Hadjidimitrakis K, Bakola S, Wong YT, Hagan MA (2019b) Mixed spatial and movement representations in the primate posterior parietal cortex. Front Neural Circuits 13:15PubMedPubMedCentral

Heider B, Jandó G, Siegel RM (2005) Functional architecture of retinotopy in visual association cortex of behaving monkey. Cereb Cortex 15:460–478PubMedPubMedCentral

Héjja-Brichard Y, Rima S, Rapha E, Durand J-B, Cottereau BR (2020) Stereomotion processing in the nonhuman primate brain. Cereb Cortex 30:4528–4543PubMed

Kaas JH, Stepniewska I (2016) Evolution of posterior parietal cortex and parietal-frontal networks for specific actions in primates. J Comp Neurol 524:595–608PubMed

Kastner S, Chen Q, Jeong SK, Mruczek REB (2017) Neuropsychologia A brief comparative review of primate posterior parietal cortex: a novel hypothesis on the human toolmaker. Neuropsychologia 105:123–134PubMedPubMedCentral

Kay KN, Winawer J, Mezer A, Wandell BA (2013) Compressive spatial summation in human visual cortex. J Neurophysiol 110:481–494PubMedPubMedCentral

Kolster H, Mandeville JB, Arsenault JT, Ekstrom LB, Wald LL, Vanduffel W (2009) Visual field map clusters in macaque extrastriate visual cortex. J Neurosci 29:7031–7039PubMedPubMedCentral

Kolster H, Janssens T, Orban GA, Vanduffel W (2014) The retinotopic organization of macaque occipitotemporal cortex anterior to V4 and caudoventral to the middle temporal (MT) cluster. J Neurosci 34:10168–10191PubMedPubMedCentral

Konen CS, Kastner S (2008) Representation of eye movements and stimulus motion in topographically organized areas of human posterior parietal cortex. J Neurosci 28:8361–8375PubMedPubMedCentral

Konen CS, Mruczek REB, Montoya JL, Kastner S (2013) Functional organization of human posterior parietal cortex: grasping- and reaching-related activations relative to topographically organized cortex. J Neurophysiol 109:2897–2908PubMedPubMedCentral

Lewis JW, Van Essen DC (2000) Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J Comp Neurol. 428:112–137PubMed

Markov NT, Ercsey-Ravasz MM, Ribeiro Gomes AR, Lamy C, Magrou L, Vezoli J, Misery P, Falchier A, Quilodran R, Gariel MA, Sallet J, Gamanut R, Huissoud C, Clavagnier S, Giroud P, Sappey-Marinier D, Barone P, Dehay C, Toroczkai Z, Knoblauch K, Van Essen DC, Kennedy H (2014) A weighted and directed interareal connectivity matrix for macaque cerebral cortex. Cereb Cortex 24:17–36PubMed

Orban GA (2016) Functional definitions of parietal areas in human and non-human primates. Proc Biol Sci 283:20160118PubMedPubMedCentral

Orban GA, Van Essen D, Vanduffel W (2004) Comparative mapping of higher visual areas in monkeys and humans. Trends Cogn Sci 8:315–324PubMed

Orban GA, Claeys K, Nelissen K, Smans R, Sunaert S, Todd JT, Wardak C, Durand JB, Vanduffel W (2006) Mapping the parietal cortex of human and non-human primates. Neuropsychologia 44:2647–2667PubMed

Pandya DN, Seltzer B (1982) Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. J Comp Neurol 204:196–210PubMed

Patel GH, Shulman GL, Baker JT, Akbudak E, Snyder AZ, Snyder LH, Corbetta M (2010) Topographic organization of macaque area LIP. Proc Natl Acad Sci USA 107:4728–4733PubMed

Pitzalis S, Galletti C, Huang RS, Patria F, Committeri G, Galati G, Fattori P, Sereno MI (2006) Wide-field retinotopy defines human cortical visual area v6. J Neurosci 26:7962–7973PubMedPubMedCentral

Pitzalis S, Sereno MI, Committeri G, Fattori P, Galati G, Tosoni A, Galletti C (2013) The human homologue of macaque area V6A. Neuroimage 82:517–530PubMed

Premereur E, Van Dromme IC, Romero MC, Vanduffel W, Janssen P (2015) Effective connectivity of depth-structure–selective patches in the lateral bank of the macaque intraparietal sulcus. PLoS Biol 13:1–20

Press WA, Brewer AA, Dougherty RF, Wade AR, Wandell BA (2001) Visual areas and spatial summation in human visual cortex. Vision Res 41:1321–1332PubMed

Rosenberg A, Cowan NJ, Angelaki DE (2013) the visual representation of 3D object orientation in parietal cortex. J Neurosci 33:19352–19361PubMedPubMedCentral

Schluppeck D, Glimcher P, Heeger DJ (2005) Topographic organization for delayed saccades in human posterior parietal cortex. J Neurophysiol 94:1372–1384PubMedPubMedCentral

Sereno MI, Tootell RBH (2005) From monkeys to humans: what do we now know about brain homologies? Curr Opin Neurobiol 15:135–144PubMed

Sereno M, Dale A, Reppas J, Kwong K, Belliveau J, Brady T, Rosen B, Tootell R (1995) Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268:889–893

Sereno MI, Pitzalis S, Martinez A (2001) Mapping of contralateral space in retinotopic coordinates by a parietal cortical area in humans. Science 294:1350–1354PubMed

Shikata E, McNamara A, Sprenger A, Hamzei F, Glauche V, Büchel C, Binkofski F (2008) Localization of human intraparietal areas AIP, CIP, and LIP using surface orientation and saccadic eye movement tasks. Hum Brain Mapp 29:411–421PubMed

Silver MA, Kastner S (2009) Topographic maps in human frontal and parietal cortex. Trends Cogn Sci 105:123–134

Silver MA, Ress D, Heeger DJ, Michael A, Topographic DJH (2005) Topographic maps of visual spatial attention in human parietal cortex. J Neurophysiol 94:1358–1371PubMedPubMedCentral

Swisher JD, Halko MA, Merabet LB, McMains SA, Somers DC (2007) Visual topography of human intraparietal sulcus. J Neurosci 27:5326–5337PubMedPubMedCentral

Tsao DY, Vanduffel W, Sasaki Y, Fize D, Knutsen TA, Mandeville JB, Wald LL, Dale AM, Rosen BR, Essen DC, Livingstone MS, Orban GA, Tootell RBH, Louis S (2003) Stereopsis activates V3A and caudal intraparietal areas in macaques and humans. Neuron 39:555–568

Tsutsui KI, Taira M, Sakata H (2005) Neural mechanisms of three-dimensional vision. Neurosci Res 51:221–229PubMed

Van Dromme IC, Premereur E, Verhoef BE, Vanduffel W, Janssen P (2016) Posterior parietal cortex drives inferotemporal activations during three-dimensional object vision. PLoS Biol 14:1–26

Van Essen DC (2004) Organization of visual areas in macaque and human cerebral cortex. In: Chalupa L, Werner J (eds) The visual neurosciences. MIT Press, Cambridge, pp 507–521

Van Essen DC, Zeki SM (1978) The topographic organization of rhesus monkey prestriate cortex. J Physiol 277:193–226PubMedPubMedCentral

Van Essen DC, Drury HA, Dickson J, Harwell J, Hanlon D, Anderson CH (2001) An integrated software suite for surface-based analyses of cerebral cortex. J Am Med Inform Assoc 8:443–459PubMedPubMedCentral

Wandell BA, Dumoulin SO, Brewer AA (2007) Visual field maps in human cortex. Neuron 56:366–383PubMed

Zhu Q, Vanduffel W (2019) Submillimeter fMRI reveals a layout of dorsal visual cortex in macaques, remarkably similar to New World monkeys. Proc Natl Acad Sci USA 116:2306–2311PubMed

Title: Wide-field retinotopy reveals a new visuotopic cluster in macaque posterior parietal cortex
Authors: Samy Rima
Benoit R. Cottereau
Yseut Héjja-Brichard
Yves Trotter
Jean-Baptiste Durand
Publication date: 01-11-2020
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 8/2020
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-020-02134-2

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Wide-field retinotopy reveals a new visuotopic cluster in macaque posterior parietal cortex

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