Topographic patterns of V2 cortical connections in macaque monkeys

Patterns of connections of dorsal and ventral portions of the second visual area (V2) were used to evaluate and extend current theories of cortical organization and processing streams in macaque monkeys. Injections of wheat germ agglutinin‐horseradish peroxidase (WGA‐HRP) and up to four different fluorochromes in V2 labeled neurons and terminations in V2 and in 1) caudal (DLc) and rostral (DLr) subdivisions of dorsolateral cortex between V2 and the middle temporal area (MT); 2) regions we define as dorsomedial (DM) and dorsointermediate (DI) areas; 3) MT, medial superior temporal area (MST), and fundal superior temporal area (FST); 4) the dorsal part of inferior temporal (TEO) cortex; and 5) two locations in posterior parietal cortex. The largest extrastriate connection zone was DLc, which occupied the caudal one‐third to one‐half of the fourth visual area (V4) region of other proposals. Based on the connection pattern, foveal vision in DLc is represented adjacent to foveal vision in V2, with the lower quadrant represented dorsally and the upper quadrant ventrally, as in V2, but within a much less extensive region of cortex. The sparser connections of DLr formed a more compressed but parallel visuotopic pattern. A third visuotopic pattern of connections was located in a moderately myelinated region of cortex just rostral to dorsomedial V2. Whereas the region would include parts of dorsal visual area 3 (V3), V3a, and possibly other areas of other proposals, we interpret the connection pattern as reflecting a dorsomedial visual area, DM, with foveal vision represented caudolaterally and other parts of the lower and upper quadrants represented more medially and rostrally. A fourth pattern of label in dorsointermediate cortex suggested the location and organization of another visual area (DI). Most of a fifth connection pattern with MT was congruent with the known visuotopic organization of MT area, but visuotopically mismatched foci of connections were observed as well. Sparser foci of label in MST suggested a rostrodorsal representation of foveal vision, with paracentral vision represented more caudally. Separate dorsal and ventral foci of label in FST were consistent with previous evidence for dorsal (FSTd) and ventral (FSTv) visual areas. Finally, connections with TEO and posterior parietal cortex were sparse. Our results suggest that much of visual cortex organization is similar in New and Old World monkeys. © 1996 Wiley‐Liss, Inc.

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

[2]  K. Rockland,et al.  Configuration, in serial reconstruction, of individual axons projecting from area V2 to V4 in the macaque monkey. , 1992, Cerebral cortex.

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

[4]  J. Tigges,et al.  Efferent cortico‐cortical fiber connections of area 18 in the squirrel monkey (Saimiri) , 1974, The Journal of comparative neurology.

[5]  L. C. Katz,et al.  Green fluorescent latex microspheres: A new retrograde tracer , 1990, Neuroscience.

[6]  P. Davison Neuronal fibrillar proteins and axoplasmic transport , 1975, Brain Research.

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

[8]  Ellen Covey,et al.  Cortical Visual Areas of the Macaque: Possible Substrates for Pattern Recognition Mechanisms , 1985 .

[9]  S. Zeki Representation of central visual fields in prestriate cortex of monkey. , 1969, Brain research.

[10]  R. Malach,et al.  Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex , 1993, The Journal of comparative neurology.

[11]  J. Tigges,et al.  Areal and laminar distribution of neurons interconnecting the central visual cortical areas 17, 18, 19, and MT in squirrel monkey (Saimiri) , 1981, The Journal of comparative neurology.

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

[13]  L. Heimer,et al.  In vivo anterograde and retrograde axonal trnasport of the fluoresecent rhodamine-dextran-amine, Fluor-Ruby, within the CNS , 1990, Brain Research.

[14]  J. Allman,et al.  Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. , 1985, Annual review of neuroscience.

[15]  J. Kaas,et al.  Archontan Affinities as Reflected in the Visual System , 1993 .

[16]  R E Weller,et al.  Cortical projections of the dorsolateral visual area in owl monkeys: The prestriate relay to inferior temporal cortex , 1985, The Journal of comparative neurology.

[17]  John H. R. Maunsell,et al.  The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic organization , 1981, The Journal of comparative neurology.

[18]  R. Weller Two cortical visual systems in Old World and New World primates. , 1988, Progress in brain research.

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

[20]  J. Kaas,et al.  A representation of the visual field in the caudal third of the middle tempral gyrus of the owl monkey (Aotus trivirgatus). , 1971, Brain research.

[21]  R. Malach,et al.  Relationship between orientation domains, cytochrome oxidase stripes, and intrinsic horizontal connections in squirrel monkey area V2. , 1994, Cerebral cortex.

[22]  M. Wong-Riley Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

[23]  R E Weller,et al.  Subdivisions and connections of inferior temporal cortex in owl monkeys , 1987, The Journal of comparative neurology.

[24]  P. White,et al.  Ketamine--its pharmacology and therapeutic uses. , 1982, Anesthesiology.

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

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

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

[28]  C. Gross,et al.  Visual topography of striate projection zone (MT) in posterior superior temporal sulcus of the macaque. , 1981, Journal of neurophysiology.

[29]  S. Zeki,et al.  The third visual complex of rhesus monkey prestriate cortex. , 1978, The Journal of physiology.

[30]  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.

[31]  Leslie G. Ungerleider,et al.  Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  Leslie G. Ungerleider,et al.  The striate projection zone in the superior temporal sulcus of Macaca mulatta: Location and topographic organization , 1979, The Journal of comparative neurology.

[33]  J. B. Levitt,et al.  Intrinsic lattice connections of macaque monkey visual cortical area V4 , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  L Krubitzer,et al.  Convergence of processing channels in the extrastriate cortex of monkeys , 1990, Visual Neuroscience.

[35]  R E Weller,et al.  Cortical connections of the middle temporal visual area (MT) and the superior temporal cortex in owl monkeys , 1984, The Journal of comparative neurology.

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

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

[38]  R. Desimone,et al.  Prestriate afferents to inferior temporal cortex: an HRP study , 1980, Brain Research.

[39]  Leslie G. Ungerleider,et al.  Projections to the superior temporal sulcus from the central and peripheral field representations of V1 and V2 , 1986, The Journal of comparative neurology.

[40]  W. Newsome,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.

[41]  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.

[42]  M. Mishkin,et al.  OCCIPITOTEMPORAL CORTICOCORTICAL CONNECTIONS IN THE RHESUS MONKEY. , 1965, Experimental neurology.

[43]  S. Zeki,et al.  The cortical projections of foveal striate cortex in the rhesus monkey. , 1978, The Journal of physiology.

[44]  S. Zeki,et al.  Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex , 1985, Nature.

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

[46]  D. Ts'o,et al.  Visual topography in primate V2: multiple representation across functional stripes , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[48]  A. Burkhalter,et al.  Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex , 1984, Nature.

[49]  D. J. Felleman,et al.  Cortical connections of areas V3 and VP of macaque monkey extrastriate visual cortex , 1997, The Journal of comparative neurology.

[50]  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.

[51]  Leslie G. Ungerleider,et al.  Pathways for motion analysis: Cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque , 1990, The Journal of comparative neurology.

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

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

[54]  D H Hubel,et al.  Connections between layer 4B of area 17 and the thick cytochrome oxidase stripes of area 18 in the squirrel monkey , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  B. Cragg The topography of the afferent projections in the circumstriate visual cortex of the monkey studied by the Nauta method. , 1969, Vision research.

[56]  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.

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

[58]  K. Rockland,et al.  A reticular pattern of intrinsic connections in primate area V2 (area 18) , 1985, The Journal of comparative neurology.

[59]  Semir Zeki,et al.  The projections to the superior temporal sulcus from areas 17 and 18 in the rhesus monkey , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[60]  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.

[61]  J. Kaas,et al.  Retinotopic patterns of connections of area 17 with visual areas V‐II and MT in macaque monkeys , 1983, The Journal of comparative neurology.

[62]  D. Hubel,et al.  Anatomy and physiology of a color system in the primate visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  J. Kaas Human Visual Cortex: Progress and puzzles , 1995, Current Biology.

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

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

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

[67]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  J. Bullier,et al.  Anatomical segregation of two cortical visual pathways in the macaque monkey , 1990, Visual Neuroscience.

[69]  S. Zeki,et al.  Modular Connections between Areas V2 and V4 of Macaque Monkey Visual Cortex , 1989, The European journal of neuroscience.

[70]  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.

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

[72]  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.

[73]  Double representation of lower visual quadrant in prelunate gyrus of rhesus monkey. , 1983, Investigative ophthalmology & visual science.

[74]  H. Kennedy,et al.  A double-labeling investigation of the afferent connectivity to cortical areas V1 and V2 of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[75]  S. Zeki,et al.  The Organization of Connections between Areas V5 and V2 in Macaque Monkey Visual Cortex , 1989, The European journal of neuroscience.

[76]  J. B. Levitt,et al.  Intrinsic cortical connections in macaque visual area V2: Evidence for interaction between different functional streams , 1994, The Journal of comparative neurology.

[77]  K. Rockland,et al.  Cortical connections of the occipital lobe in the rhesus monkey: Interconnections between areas 17, 18, 19 and the superior temporal sulcus , 1981, Brain Research.

[78]  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.

[79]  Jon H. Kaas,et al.  Cortical projections of area 18 in owl monkeys , 1977, Vision Research.

[80]  Jon H. Kaas,et al.  The Organization of Visual Cortex in Primates: Problems, Conclusions, and the Use of Comparative Studies in Understanding the Human Brain , 1993 .

[81]  W. B. Spatz,et al.  Morphology and connections of neurons in area 17 projecting to the extrastriate areas mt and 19DM and to the superior colliculus in the monkey Callithrix jacchus , 1995, The Journal of comparative neurology.

[82]  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.

[83]  R. M. Siegel,et al.  Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule , 1990, The Journal of comparative neurology.

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

[85]  Leslie G. Ungerleider,et al.  Cortical connections of inferior temporal area TEO in macaque monkeys , 1993, The Journal of comparative neurology.

[86]  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.

[87]  R. Weller,et al.  Cortical connections of subdivisions of inferior temporal cortex in squirrel monkeys , 1992, The Journal of comparative neurology.

[88]  E. DeYoe,et al.  Segregation of efferent connections and receptive field properties in visual area V2 of the macaque , 1985, Nature.

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

[90]  J. Kaas,et al.  Cortical integration of parallel pathways in the visual system of primates , 1989, Brain Research.

[91]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.