Visual areas in lateral and ventral extrastriate cortices of the marmoset monkey

The representation of the visual field in visual areas of the dorsolateral, lateral, and ventral cortices was studied by means of extracellular recordings and fluorescent tracer injections in anaesthetised marmoset monkeys. Two areas, forming mirror‐symmetrical representations of the contralateral visual field, were found rostral to the second visual area (V2). These were termed the ventrolateral posterior (VLP) and the ventrolateral anterior (VLA) areas. In both areas, the representation of the lower quadrant is located dorsally, between the foveal representation of V2 and the middle temporal crescent (MTc), whereas the representation of the upper quadrant is located ventrally, in the supratentorial cortex. A representation of the vertical meridian forms the common border of areas VLP and VLA, whereas the horizontal meridian is represented both at the caudal border of area VLP (with V2) and at the rostral border of area VLA (with multiple extrastriate areas). The foveal representations of areas VLP and VLA are continuous with that of V2, being located at the lateral edge of the hemisphere. The topographic and laminar patterns of projections from dorsolateral and ventral cortices to the primary (V1) and dorsomedial (DM) visual areas both support the present definition of the borders of areas VLP and VLA. These results argue against a separation between dorsolateral and ventral extrastriate areas and provide clues for the likely homologies between extrastriate areas of different species. J. Comp. Neurol. 422:621–651, 2000. © 2000 Wiley‐Liss, Inc.

[1]  F. Condé.  Further studies on the use of the fluorescent tracers fast blue and diamidino yellow: Effective uptake area and cellular storage sites , 1987, Journal of Neuroscience Methods.

[2]  J. Kaas,et al.  Cortical connections of area 18 and dorsolateral visual cortex in squirrel monkeys , 1988, Visual Neuroscience.

[3]  H. Kennedy,et al.  Topography of the afferent connectivity of area 17 in the macaque monkey: A double‐labelling study , 1986, The Journal of comparative neurology.

[4]  R Gattass,et al.  Area V4 in Cebus monkey: extent and visuotopic organization. , 1998, Cerebral cortex.

[5]  G. Elston,et al.  Visuotopic organisation and neuronal response selectivity for direction of motion in visual areas of the caudal temporal lobe of the marmoset monkey (Callithrix jacchus): Middle temporal area, middle temporal crescent, and surrounding cortex , 1998, The Journal of comparative neurology.

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

[7]  J. Kaas.  Theories of visual cortex organization in primates: areas of the third level. , 1996, Progress in brain research.

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

[9]  S. Zeki.  Are areas TEO and PIT of monkey visual cortex wholly distinct from the fourth visual complex (V4 complex) ? , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  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.

[11]  Leslie G. Ungerleider,et al.  Multiple visual areas in the caudal superior temporal sulcus of the macaque , 1986, The Journal of comparative neurology.

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

[13]  R E Weller,et al.  Cortical connections of the caudal subdivision of the dorsolateral area (V4) in monkeys , 1991, The Journal of comparative neurology.

[14]  J. Kaas,et al.  Cortical connections of the dorsomedial visual area in Old World macaque monkeys , 1999, The Journal of comparative neurology.

[15]  John M. Allman,et al.  11 – The Functional Organization of Visual Cortex in Owl Monkeys , 1994 .

[16]  M. Rosa.  Visuotopic Organization of Primate Extrastriate Cortex , 1997 .

[17]  B. B. Lee,et al.  Topography of ganglion cells and photoreceptors in the retina of a New World monkey: The marmoset Callithrix jacchus , 1996, Visual Neuroscience.

[18]  J. Kaas,et al.  Topographic patterns of V2 cortical connections in macaque monkeys , 1996, The Journal of comparative neurology.

[19]  S. Zeki.  The distribution of wavelength and orientation selective cells in different areas of monkey visual cortex , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[20]  J. Kaas.  Theories of Visual Cortex Organization in Primates , 1997 .

[21]  M G Rosa,et al.  Visual areas in the dorsal and medial extrastriate cortices of the marmoset , 1995, The Journal of comparative neurology.

[22]  D. V. van Essen,et al.  Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  M I Sereno,et al.  Analysis of retinotopic maps in extrastriate cortex. , 1994, Cerebral cortex.

[24]  K. Rockland,et al.  Direct temporal-occipital feedback connections to striate cortex (V1) in the macaque monkey. , 1994, Cerebral cortex.

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

[26]  L. Schmued.  A rapid, sensitive histochemical stain for myelin in frozen brain sections. , 1990, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[27]  R Gattass,et al.  Topographic organization of cortical input to striate cortex in the Cebus monkey: A fluorescent tracer study , 1991, The Journal of comparative neurology.

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

[29]  S. Schein,et al.  Is there a high concentration of color-selective cells in area V4 of monkey visual cortex? , 1982, Journal of neurophysiology.

[30]  S Zeki,et al.  The clinical and functional measurement of cortical (in)activity in the visual brain, with special reference to the two subdivisions (V4 and V4 alpha) of the human colour centre. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[31]  M G Rosa,et al.  Visuotopic organisation of striate cortex in the marmoset monkey (Callithrix jacchus) , 1996, The Journal of comparative neurology.

[32]  W T Newsome,et al.  Ventral posterior visual area of the macaque: Visual topography and areal boundaries , 1986, The Journal of comparative neurology.

[33]  S. Zeki,et al.  Has a new color area been discovered? , 1998, Nature Neuroscience.

[34]  W T Newsome,et al.  Interhemispheric connections of visual cortex in the owl monkey, Aotus trivirgatus, and the bushbaby, Galago senegalensis , 1980, The Journal of comparative neurology.

[35]  S. Zeki.  Cortical projections from two prestriate areas in the monkey. , 1971, Brain research.

[36]  Leslie G. Ungerleider,et al.  Cortical connections of visual area MT in the macaque , 1986, The Journal of comparative neurology.

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

[38]  Paul R. Martin,et al.  Temporal contrast sensitivity in the lateral geniculate nucleus of a New World monkey, the marmoset Callithrix jacchus , 1999, The Journal of physiology.

[39]  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.

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

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

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

[43]  M G Rosa,et al.  Cellular heterogeneity in cerebral cortex: A study of the morphology of pyramidal neurones in visual areas of the marmoset monkey , 1999, The Journal of comparative neurology.

[44]  W. Maguire,et al.  Visuotopic organization of the prelunate gyrus in rhesus monkey , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  A. Goodchild,et al.  Segregation of receptive field properties in the lateral geniculate nucleus of a New-World monkey, the marmoset Callithrix jacchus. , 1998, Journal of neurophysiology.

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

[47]  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.

[48]  C Blakemore,et al.  Functional architecture of area 17 in normal and monocularly deprived marmosets (Callithrix jacchus) , 1996, Visual Neuroscience.

[49]  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.

[50]  G. Elston,et al.  The second visual area in the marmoset monkey: Visuotopic organisation, magnification factors, architectonical boundaries, and modularity , 1997, The Journal of comparative neurology.

[51]  A. Morel,et al.  Connections of visual areas of the upper temporal lobe of owl monkeys: the MT crescent and dorsal and ventral subdivisions of FST , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  Leslie G. Ungerleider,et al.  Cortical projections of area V2 in the macaque. , 1997, Cerebral cortex.