Cortical connections of areas V3 and VP of macaque monkey extrastriate visual cortex

The cortical connections of visual area 3 (V3) and the ventral posterior area (VP) in the macaque monkey were studied by using combinations of retrograde and anterograde tracers. Tracer injections were made into V3 or VP following electrophysiological recording in and near the target area. The pattern of ipsilateral cortical connections was analyzed in relation to the pattern of interhemispheric connections identified after transection of the corpus callosum. Both V3 and VP have major connections with areas V2, V3A, posterior intraparietal area (PIP), V4, middle temporal area (MT), medial superior temporal area (dorsal) (MSTd), and ventral intraparietal area (VIP). Their connections differ in several respects. Specifically, V3 has connections with areas V1 and V4 transitional area (V4t) that are absent for VP; VP has connections with areas ventral occipitotemporal area (VOT), dorsal prelunate area (DP), and visually responsive portion of temporal visual area F (VTF) that are absent or occur only rarely for V3. The laminar pattern of labeled terminals and retrogradely labeled cell bodies allowed assessment of the hierarchical relationships between areas V3 and VP and their various targets. Areas V1 and V2 are at a lower hierarchical level than V3 and VP; all of the remaining areas are at a higher level. V3 receives major inputs from layer 4B of V1, suggesting an association with the magnocellular‐dominated processing stream and a role in routing magnocellular‐dominated information along pathways leading to both parietal and temporal lobes. The convergence and divergence of pathways involving V3 and VP underscores the distributed nature of hierarchical processing in the visual system. J. Comp. Neurol. 379:21‐47, 1997. © 1997 Wiley‐Liss, Inc.

[1]  L. Krubitzer The organization of neocortex in mammals: are species differences really so different? , 1995, Trends in Neurosciences.

[2]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[3]  J. Morrison,et al.  Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis , 1995, The Journal of comparative neurology.

[4]  E. DeYoe,et al.  Concurrent processing in the primate visual cortex. , 1995 .

[5]  P A Salin,et al.  Corticocortical connections in the visual system: structure and function. , 1995, Physiological reviews.

[6]  V. Casagrande A third parallel visual pathway to primate area V1 , 1994, Trends in Neurosciences.

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

[8]  D. V. Essen,et al.  Neural mechanisms of form and motion processing in the primate visual system , 1994, Neuron.

[9]  David C. Van Essen,et al.  Multiple processing streams in occipitotemporal visual cortex , 1994, Nature.

[10]  Leslie G. Ungerleider,et al.  The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  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.

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

[13]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[14]  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.

[15]  C. Colby,et al.  Heterogeneity of extrastriate visual areas and multiple parietal areas in the Macaque monkey , 1991, Neuropsychologia.

[16]  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.

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

[18]  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.

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

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

[21]  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.

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

[23]  D. Ts'o,et al.  Functional organization of primate visual cortex revealed by high resolution optical imaging. , 1990, Science.

[24]  D. V. van Essen,et al.  Antibody labeling of functional subdivisions in visual cortex: Cat-301 immunoreactivity in striate and extrastriate cortex of the macaque monkey , 1990, Visual Neuroscience.

[25]  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.

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

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

[28]  D. C. Essen,et al.  Modular and hierarchical organization of extrastriate visual cortex in the macaque monkey. , 1990, Cold Spring Harbor symposia on quantitative biology.

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

[30]  R. Tootell,et al.  Functional anatomy of the second visual area (V2) in the macaque , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[32]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. , 1988, Journal of neurophysiology.

[33]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. III. Interaction with full-field visual stimulation. , 1988, Journal of neurophysiology.

[34]  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.

[35]  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.

[36]  John H. R. Maunsell,et al.  Topographic organization of the middle temporal visual area in the macaque monkey: Representational biases and the relationship to callosal connections and myeloarchitectonic boundaries , 1987, The Journal of comparative neurology.

[37]  D. J. Felleman,et al.  Receptive field properties of neurons in area V3 of macaque monkey extrastriate cortex. , 1987, Journal of neurophysiology.

[38]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

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

[40]  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.

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

[42]  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.

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

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

[45]  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.

[46]  S. Levay,et al.  The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[48]  John H. R. Maunsell,et al.  The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability , 1984, Vision Research.

[49]  D. Hubel,et al.  Specificity of intrinsic connections in primate primary visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  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.

[51]  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.

[52]  D C Van Essen,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. , 1983, Journal of neurophysiology.

[53]  D. V. van Essen,et al.  The pattern of interhemispheric connections and its relationship to extrastriate visual areas in the macaque monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  Dean Falk,et al.  Primate Brain Evolution: Methods and Concepts , 1982 .

[55]  J. Allman Reconstructing the Evolution of the Brain in Primates Through the Use of Comparative Neurophysiological and Neuroanatomical Data , 1982 .

[56]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

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

[58]  H. Barbas,et al.  Organization of afferent input to subdivisions of area 8 in the rhesus monkey , 1981, The Journal of comparative neurology.

[59]  R. Desimone,et al.  Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. , 1981, Journal of neurophysiology.

[60]  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.

[61]  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.

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

[63]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

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

[65]  J. Kaas,et al.  Double representation of the body surface within cytoarchitectonic area 3b and 1 in “SI” in the owl monkey (aotus trivirgatus) , 1978, The Journal of comparative neurology.

[66]  S. Zeki Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. , 1978, The Journal of physiology.

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

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

[69]  D. Pandya,et al.  Limbic and sensory connections of the inferior parietal lobule (area PG) in the rhesus monkey: A study with a new method for horseradish peroxidase histochemistry , 1977, Brain Research.

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

[71]  J. Allman,et al.  The dorsomedial cortical visual area: A third tier area in the occipital lobe of the owl monkey (aotus trivirgatus) , 1975, Brain Research.

[72]  A. Hendrickson,et al.  The autoradiographic demonstration of axonal connections in the central nervous system. , 1972, Brain research.

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

[74]  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.

[75]  S. Zeki Interhemispheric connections of prestriate cortex in monkey. , 1970, Brain research.

[76]  J. Häggendal,et al.  Noradrenaline and dopamine content in the brain of the cockroach Periplaneta americana. , 1969, Brain research.

[77]  J. T. Wiitanen,et al.  Selective silver impregnation of degenerating axons and axon terminals in the central nervous system of the monkey (Macaca mulatta). , 1969, Brain research.

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

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