Visual areas in the dorsal and medial extrastriate cortices of the marmoset

To define the number and limits of the visual areas in the primate extrastriate cortex, the visuotopy of the dorsal convexity and medial wall was studied by electrophysiological recordings in five marmosets anaesthetised with sufentanil and nitrous oxide and paralysed with pancuronium bromide. We identified five visuotopic representations in and around the densely myelinated zone between visual area 2 (V2) and the posterior parietal cortex. Most of the densely myelinated zone is formed by the homologue of the owl monkey's dorsomedial area (DM); thus, we also termed this area DM in the marmoset. Within DM, the lower quadrant representation is continuous, with central vision represented laterally, peripheral vision medially, the horizontal meridian caudally, and the vertical meridian rostrally. In contrast, the upper quadrant representation is split, with the central portion represented at the lateral edge of DM on the dorsal surface, and the periphery along the midline. Two other visual field representations, corresponding to the dorsointermediate area (DI) and to a new subdivision termed the dorsoanterior area (DA), are also densely myelinated but can be distinguished from DM based on the separation of the bands of Baillerger and visual topography. In addition, a homologue of the medial visual area (M) was identified. Our results reveal a highly complex visuotopy in primate cortex, with local discontinuities in representation and borders between areas that are often not coincident with either the horizontal or the vertical meridian. The topography of the dorsal extrastriate cortex in the marmoset strongly suggests that both visual area 3 (V3) and the parieiooccipital area (PO) of other primates are portions of a single visuotopic representation, DM, and calls into question the, existence of visual areas with partial or quadrantic representations of the visual field. © 1995 Wiley‐Liss, Inc.

[1]  David Troilo,et al.  Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus) , 1993, Vision Research.

[2]  M. Rosa,et al.  Responsiveness of cat area 17 after monocular inactivation: limitation of topographic plasticity in adult cortex. , 1995, The Journal of physiology.

[3]  M G Rosa,et al.  Retinotopic orgarnzation of the primary visual cortex of flying foxes (Pteropus poliocephalus and pteropus scapulatus) , 1993, The Journal of comparative neurology.

[4]  P A Salin,et al.  Visual activity in areas V3a and V3 during reversible inactivation of area V1 in the macaque monkey. , 1991, Journal of neurophysiology.

[5]  J. Kaas,et al.  Representation of the visual field on the medial wall of occipital-parietal cortex in the owl monkey. , 1976, Science.

[6]  V. Montero Topography of the cortico-cortical connections from the striate cortex in the cat. , 1981, Brain, behavior and evolution.

[7]  The Auditory Cortex , 1982 .

[8]  L A Krubitzer,et al.  Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns , 1990, Visual Neuroscience.

[9]  M G Rosa,et al.  Topography and extent of visual-field representation in the superior colliculus of the megachiropteran Pteropus , 1994, Visual Neuroscience.

[10]  J G Malpeli,et al.  Global form and singularity: modeling the blind spot's role in lateral geniculate morphogenesis. , 1994, Science.

[11]  R. Andersen,et al.  Visual receptive field organization and cortico‐cortical connections of the lateral intraparietal area (area LIP) in the macaque , 1990, The Journal of comparative neurology.

[12]  Leslie G. Ungerleider,et al.  Visual topography of area TEO in the macaque , 1991, The Journal of comparative neurology.

[13]  M. Silverman,et al.  Functional organization of the second cortical visual area in primates. , 1983, Science.

[14]  Martin I. Sereno,et al.  Cortical visual areas in mammals , 1991 .

[15]  K. Albus,et al.  Second and third visual areas of the cat: interindividual variability in retinotopic arrangement and cortical location , 1980, The Journal of physiology.

[16]  R. Weller,et al.  Cortical connections of dorsal cortex rostral to V II in squirrel monkeys , 1991, The Journal of comparative neurology.

[17]  R Gattass,et al.  Cortical afferents of visual area MT in the Cebus monkey: Possible homologies between New and old World monkeys , 1993, Visual Neuroscience.

[18]  J. Maunsell,et al.  Two‐dimensional maps of the cerebral cortex , 1980, The Journal of comparative neurology.

[19]  C. Galletti,et al.  Functional Properties of Neurons in the Anterior Bank of the Parieto‐occipital Sulcus of the Macaque Monkey , 1991, The European journal of neuroscience.

[20]  H. Sherk,et al.  A reassessment of the lower visual field map in striate-recipient lateral suprasylvian cortex , 1993, Visual Neuroscience.

[21]  L A Krubitzer,et al.  The dorsomedial visual area of owl monkeys: Connections, myeloarchitecture, and homologies in other primates , 1993, The Journal of comparative neurology.

[22]  J. Pettigrew,et al.  Organization of the second visual area in the megachiropteran bat Pteropus. , 1994, Cerebral cortex.

[23]  L. Palmer,et al.  Retinotopic organization of areas 20 and 21 in the cat , 1980, The Journal of comparative neurology.

[24]  A. Cowey,et al.  Preferential representation of the fovea in the primary visual cortex , 1993, Nature.

[25]  C. Gross,et al.  Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: A dual tracer study , 1988, The Journal of comparative neurology.

[26]  D. J. Felleman,et al.  Anatomical and physiological asymmetries related to visual areas V3 and VP in macaque extrastriate cortex , 1986, Vision Research.

[27]  D. Whitteridge,et al.  The representation of the visual field on the cerebral cortex in monkeys , 1961, The Journal of physiology.

[28]  J. Kaas,et al.  The organization of the second visual area (V II) in the owl monkey: a second order transformation of the visual hemifield. , 1974, Brain research.

[29]  D. Hubel,et al.  Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey , 1981, Nature.

[30]  L. Krubitzer,et al.  Five topographically organized fields in the somatosensory cortex of the flying fox: Microelectrode maps, myeloarchitecture, and cortical modules , 1992, The Journal of comparative neurology.

[31]  L. Palmer,et al.  Retinotopic organization of areas 18 and 19 in the cat , 1979, The Journal of comparative neurology.

[32]  C. Gross,et al.  Visual topography of V2 in the macaque , 1981, The Journal of comparative neurology.

[33]  S Shipp,et al.  Visuotopic organization of the lateral suprasylvian area and of an adjacent area of the ectosylvian gyrus of cat cortex: A physioligical and connectional study , 1991, Visual Neuroscience.

[34]  John H. R. Maunsell,et al.  The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: Asymmetries, areal boundaries, and patchy connections , 1986, The Journal of comparative neurology.

[35]  V. Perry,et al.  The retinal ganglion cell distribution and the representation of the visual field in area 17 of the owl monkey, Aotus trivirgatus , 1993, Visual Neuroscience.

[36]  L. Palmer,et al.  The retinotopic organization of area 17 (striate cortex) in the cat , 1978, The Journal of comparative neurology.

[37]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[38]  W. Burke,et al.  Processing of form and motion in area 21a of cat visual cortex , 1993, Visual Neuroscience.

[39]  R Gattass,et al.  Identification and viuotopic organization of areas PO and POd in Cebus monkey , 1994, The Journal of comparative neurology.

[40]  J. Allman,et al.  The dorsal third tier area inGalago senegalensis , 1979, Brain Research.

[41]  J. Kaas,et al.  A crescent-shaped cortical visual area surrounding the middle temporal area (MT) in the owl monkey (Aotus trivirgatus). , 1974, Brain research.

[42]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: anatomic location and visual response properties. , 1993, Journal of neurophysiology.

[43]  R. Dykes Parallel processing of somatosensory information: A theory , 1983, Brain Research Reviews.

[44]  Roger B. H. Tootell,et al.  Segregation of global and local motion processing in primate middle temporal visual area , 1992, Nature.

[45]  H. Sherk Location and connections of visual cortical areas in the cat's suprasylvian sulcus , 1986, The Journal of comparative neurology.

[46]  D. C. Essen,et al.  The topographic organization of rhesus monkey prestriate cortex. , 1978, The Journal of physiology.

[47]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[48]  J. Kaas,et al.  The dorsomedial cortical visual area: a third tier area in the occipital lobe of the owl monkey (Aotus trivirgatus). , 1975 .

[49]  F. Previc Functional specialization in the lower and upper visual fields in humans: Its ecological origins and neurophysiological implications , 1990, Behavioral and Brain Sciences.

[50]  R Gattass,et al.  Representation of the visual field in the second visual area in the Cebus monkey , 1988, The Journal of comparative neurology.

[51]  C. Gross,et al.  Visuotopic organization and extent of V3 and V4 of the macaque , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.