Diversity and Cell Type Specificity of Local Excitatory Connections to Neurons in Layer 3B of Monkey Primary Visual Cortex

In the primary visual cortex of macaque monkeys, laminar and columnar axonal specificity are correlated with functional differences between locations. We describe evidence that embedded within this anatomical framework is finer specificity of functional connections. Photostimulation-based mapping of functional input to 31 layer 3B neurons revealed that input sources to individual cells were highly diverse. Although some input differences were correlated with neuronal anatomy, no 2 neurons received excitatory input from the same cortical layers. Thus, input diversity reveals far more cell types than does anatomical diversity. This implies relatively little functional redundancy; despite trends related to laminar or columnar position, pools of neurons contributing uniquely to visual processing are likely relatively small. These results also imply that similarities in the anatomy of circuits in different cortical areas or species may not indicate similar functional connectivity.

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

[2]  Arnold R. Kriegstein,et al.  Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex , 1989, Journal of Neuroscience Methods.

[3]  V. Casagrande,et al.  Parallel pathways in macaque monkey striate cortex: anatomically defined columns in layer III. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[6]  J. Lund,et al.  Local circuit neurons of macaque monkey striate cortex: III. Neurons of laminae 4B, 4A, and 3B , 1997, The Journal of comparative neurology.

[7]  S. Zeki,et al.  Segregation and convergence of specialised pathways in macaque monkey visual cortex. , 1995, Journal of anatomy.

[8]  E. Callaway,et al.  Cytochrome-oxidase blobs and intrinsic horizontal connections of layer 2/3 pyramidal neurons in primate V1 , 1998, Visual Neuroscience.

[9]  Lawrence C. Katz,et al.  Scanning laser photostimulation: a new approach for analyzing brain circuits , 1994, Journal of Neuroscience Methods.

[10]  M. Cynader,et al.  Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). , 1992, Cerebral cortex.

[11]  E. Callaway,et al.  Contributions of individual layer 2–5 spiny neurons to local circuits in macaque primary visual cortex , 1996, Visual Neuroscience.

[12]  Richard H Masland,et al.  Extreme Diversity among Amacrine Cells: Implications for Function , 1998, Neuron.

[13]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. V. Spatial frequency , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  D. Hubel,et al.  Segregation of form, color, movement, and depth: anatomy, physiology, and perception. , 1988, Science.

[15]  C. Stevens,et al.  Neuronal diversity: Too many cell types for comfort? , 1998, Current Biology.

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

[17]  D. Hubel,et al.  Sequence regularity and geometry of orientation columns in the monkey striate cortex , 1974, The Journal of comparative neurology.

[18]  DH Hubel,et al.  Segregation of form, color, and stereopsis in primate area 18 , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[20]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[21]  E. Callaway,et al.  Contributions of individual layer 6 pyramidal neurons to local circuitry in macaque primary visual cortex , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  M. Dalva,et al.  Rearrangements of synaptic connections in visual cortex revealed by laser photostimulation. , 1994, Science.

[23]  E. Callaway Local circuits in primary visual cortex of the macaque monkey. , 1998, Annual review of neuroscience.

[24]  J. B. Levitt,et al.  Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: Anatomy of interlaminar projections , 1994, Visual Neuroscience.

[25]  J. B. Levitt,et al.  Receptive fields and functional architecture of macaque V2. , 1994, Journal of neurophysiology.

[26]  L. Benevento,et al.  Demonstration of lack of dorsal lateral geniculate nucleus input to extrastriate areas MT and Visual 2 in the macaque monkey , 1982, Brain Research.

[27]  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.

[28]  Masao Yukie,et al.  Laminar origin of direct projection from cortex area V1 to V4 in the rhesus monkey , 1985, Brain Research.

[29]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[30]  E. Callaway,et al.  Convergence of magno- and parvocellular pathways in layer 4B of macaque primary visual cortex , 1996, Nature.

[31]  E. Callaway,et al.  Functional Streams and Local Connections of Layer 4C Neurons in Primary Visual Cortex of the Macaque Monkey , 1998, The Journal of Neuroscience.

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

[33]  R. Malach,et al.  Dendritic sampling across processing streams in monkey striate cortex , 1992, The Journal of comparative neurology.

[34]  J. Lund Local circuit neurons of macaque monkey striate cortex: I. Neurons of laminae 4C and 5A , 1987, The Journal of comparative neurology.

[35]  J C Anderson,et al.  Form, function, and intracortical projections of neurons in the striate cortex of the monkey Macacus nemestrinus. , 1993, Cerebral cortex.

[36]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. III. Color , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[38]  K. Purpura,et al.  Contrast sensitivity and spatial frequency response of primate cortical neurons in and around the cytochrome oxidase blobs , 1995, Vision Research.

[39]  E. Callaway,et al.  Photostimulation using caged glutamate reveals functional circuitry in living brain slices. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[40]  D. Hubel,et al.  Specificity of cortico-cortical connections in monkey visual system , 1983, Nature.

[41]  R. Miles,et al.  How Many Subtypes of Inhibitory Cells in the Hippocampus? , 1998, Neuron.

[42]  T. Wiesel,et al.  Local circuits and ocular dominance columns in monkey striate cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  A. Parker,et al.  Local circuit neurons of macaque monkey striate cortex: II. Neurons of laminae 5B and 6 , 1988, The Journal of comparative neurology.

[44]  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.

[45]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. I. Ocular dominance, binocular interactions, and baseline conditions , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[47]  J. Bolz,et al.  Relationships between dendritic morphology and cytochrome oxidase compartments in monkey striate cortex , 1992, The Journal of comparative neurology.

[48]  J. Bullier,et al.  Parallel versus serial processing: new vistas on the distributed organization of the visual system , 1995, Current Opinion in Neurobiology.

[49]  T. Wiesel,et al.  Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.