Receptive fields and functional architecture of macaque V2

J. B. Levitt, D. C. Kiper, J. Anthony Movshon

Research output: Contribution to journalArticle

Abstract

1. Visual area V2 of macaque monkey cerebral cortex is the largest of the extrastriate visual areas, yet surprisingly little is known of its neuronal properties. We have made a quantitative analysis of V2 receptive field properties. Our set of measurements was chosen to distinguish neuronal responses reflecting parvocellular (P) or magnocellular (M) inputs and to permit comparison with similar measurements made in other visual areas; we further describe the relationship of those properties to the laminar and cytochrome oxidase (CO) architecture of V2. 2. We recorded the activity of single units representing the central 5° in all laminae and CO divisions of V2 in anesthetized, paralyzed macaque monkeys. We studied responses to geometric targets and to drifting sinusoidal gratings that varied in orientation, spatial frequency, drift rate, contrast, and color. 3. The orientation selectivity and spatial and temporal tuning of V2 neurons differed little from those in V1. As in V1, spatial and temporal tuning in V2 appeared separable, and we identified a population of simple cells (more common within the central 3°) similar to those found in V1. Contrast sensitivity of V2 neurons was greater on average than in V1, perhaps reflecting the summation of inputs in V2's larger receptive fields. Many V2 neurons exhibited some degree of chromatic opponency, responding to isoluminant color variations, but these neurons differed from V1 in the linearity with which they summate cone signals. 4. In agreement with others, we found that neurons with selective responses to color, size, and motion did seem to cluster in different CO compartments. However, this segregation of qualitatively different response selectivities was not absolute, and response properties also seemed to depend on laminar position within each compartment. As others also have noted, we found that CO stripe widths in the macaque (unlike in the squirrel monkey) did not consistently appear different. We relied on the segregation of qualitatively distinct cell types, and in some cases the pattern of Cat-301 staining as well, to distinguish CO stripes when the staining pattern of CO alone was ambiguous. Although all cell types were found in all CO compartments and laminae, unoriented cells were more prominent in layers 2-4 of 'thin' stripes, direction-selective cells in layers 3B/4 of 'thick' stripes, color-selective cells in the upper layers of thin and pale stripes, and end-stopped cells mainly outside of layer 4 in thin stripes. 5. Cells in the different CO compartments differed little in their spatial, temporal, and contrast sensitivity or in their orientation selectivity, although thin-stripe cells more commonly were unoriented and had somewhat lower spatial resolution and contrast sensitivity than did cells in thick and pale stripes. Thus whereas our results are broadly consistent with functional segregation across V2, they also suggest that the physiological organization of V2 is substantially more homogeneous than has been previously appreciated and are inconsistent with continued segregation of P and M signals in V2.

Original languageEnglish (US)
Pages (from-to)2517-2542
Number of pages26
JournalJournal of Neurophysiology
Volume71
Issue number6
StatePublished - 1994

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Macaca
Electron Transport Complex IV
Color
Contrast Sensitivity
Neurons
Haplorhini
Staining and Labeling
Saimiri
Cerebral Cortex
Cats

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Receptive fields and functional architecture of macaque V2. / Levitt, J. B.; Kiper, D. C.; Movshon, J. Anthony.

In: Journal of Neurophysiology, Vol. 71, No. 6, 1994, p. 2517-2542.

Research output: Contribution to journalArticle

Levitt, J. B. ; Kiper, D. C. ; Movshon, J. Anthony. / Receptive fields and functional architecture of macaque V2. In: Journal of Neurophysiology. 1994 ; Vol. 71, No. 6. pp. 2517-2542.
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abstract = "1. Visual area V2 of macaque monkey cerebral cortex is the largest of the extrastriate visual areas, yet surprisingly little is known of its neuronal properties. We have made a quantitative analysis of V2 receptive field properties. Our set of measurements was chosen to distinguish neuronal responses reflecting parvocellular (P) or magnocellular (M) inputs and to permit comparison with similar measurements made in other visual areas; we further describe the relationship of those properties to the laminar and cytochrome oxidase (CO) architecture of V2. 2. We recorded the activity of single units representing the central 5° in all laminae and CO divisions of V2 in anesthetized, paralyzed macaque monkeys. We studied responses to geometric targets and to drifting sinusoidal gratings that varied in orientation, spatial frequency, drift rate, contrast, and color. 3. The orientation selectivity and spatial and temporal tuning of V2 neurons differed little from those in V1. As in V1, spatial and temporal tuning in V2 appeared separable, and we identified a population of simple cells (more common within the central 3°) similar to those found in V1. Contrast sensitivity of V2 neurons was greater on average than in V1, perhaps reflecting the summation of inputs in V2's larger receptive fields. Many V2 neurons exhibited some degree of chromatic opponency, responding to isoluminant color variations, but these neurons differed from V1 in the linearity with which they summate cone signals. 4. In agreement with others, we found that neurons with selective responses to color, size, and motion did seem to cluster in different CO compartments. However, this segregation of qualitatively different response selectivities was not absolute, and response properties also seemed to depend on laminar position within each compartment. As others also have noted, we found that CO stripe widths in the macaque (unlike in the squirrel monkey) did not consistently appear different. We relied on the segregation of qualitatively distinct cell types, and in some cases the pattern of Cat-301 staining as well, to distinguish CO stripes when the staining pattern of CO alone was ambiguous. Although all cell types were found in all CO compartments and laminae, unoriented cells were more prominent in layers 2-4 of 'thin' stripes, direction-selective cells in layers 3B/4 of 'thick' stripes, color-selective cells in the upper layers of thin and pale stripes, and end-stopped cells mainly outside of layer 4 in thin stripes. 5. Cells in the different CO compartments differed little in their spatial, temporal, and contrast sensitivity or in their orientation selectivity, although thin-stripe cells more commonly were unoriented and had somewhat lower spatial resolution and contrast sensitivity than did cells in thick and pale stripes. Thus whereas our results are broadly consistent with functional segregation across V2, they also suggest that the physiological organization of V2 is substantially more homogeneous than has been previously appreciated and are inconsistent with continued segregation of P and M signals in V2.",
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N2 - 1. Visual area V2 of macaque monkey cerebral cortex is the largest of the extrastriate visual areas, yet surprisingly little is known of its neuronal properties. We have made a quantitative analysis of V2 receptive field properties. Our set of measurements was chosen to distinguish neuronal responses reflecting parvocellular (P) or magnocellular (M) inputs and to permit comparison with similar measurements made in other visual areas; we further describe the relationship of those properties to the laminar and cytochrome oxidase (CO) architecture of V2. 2. We recorded the activity of single units representing the central 5° in all laminae and CO divisions of V2 in anesthetized, paralyzed macaque monkeys. We studied responses to geometric targets and to drifting sinusoidal gratings that varied in orientation, spatial frequency, drift rate, contrast, and color. 3. The orientation selectivity and spatial and temporal tuning of V2 neurons differed little from those in V1. As in V1, spatial and temporal tuning in V2 appeared separable, and we identified a population of simple cells (more common within the central 3°) similar to those found in V1. Contrast sensitivity of V2 neurons was greater on average than in V1, perhaps reflecting the summation of inputs in V2's larger receptive fields. Many V2 neurons exhibited some degree of chromatic opponency, responding to isoluminant color variations, but these neurons differed from V1 in the linearity with which they summate cone signals. 4. In agreement with others, we found that neurons with selective responses to color, size, and motion did seem to cluster in different CO compartments. However, this segregation of qualitatively different response selectivities was not absolute, and response properties also seemed to depend on laminar position within each compartment. As others also have noted, we found that CO stripe widths in the macaque (unlike in the squirrel monkey) did not consistently appear different. We relied on the segregation of qualitatively distinct cell types, and in some cases the pattern of Cat-301 staining as well, to distinguish CO stripes when the staining pattern of CO alone was ambiguous. Although all cell types were found in all CO compartments and laminae, unoriented cells were more prominent in layers 2-4 of 'thin' stripes, direction-selective cells in layers 3B/4 of 'thick' stripes, color-selective cells in the upper layers of thin and pale stripes, and end-stopped cells mainly outside of layer 4 in thin stripes. 5. Cells in the different CO compartments differed little in their spatial, temporal, and contrast sensitivity or in their orientation selectivity, although thin-stripe cells more commonly were unoriented and had somewhat lower spatial resolution and contrast sensitivity than did cells in thick and pale stripes. Thus whereas our results are broadly consistent with functional segregation across V2, they also suggest that the physiological organization of V2 is substantially more homogeneous than has been previously appreciated and are inconsistent with continued segregation of P and M signals in V2.

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