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The influence of input from the lower cortical layers on the orientation tuning of upper layer V1 cells in a primate

Published online by Cambridge University Press:  02 June 2009

John D. Allison
Affiliation:
Department of Cell Biology, Vanderbilt University, Nashville
Vivien A. Casagrande
Affiliation:
Department of Cell Biology, Vanderbilt University, Nashville Department of Psychology, Vanderbilt University, Nashville
A.B. Bonds
Affiliation:
Department of Electrical and Biomedical Engineering, Vanderbilt University, Nashville

Abstract

The receptive fields of cells in the primary visual cortex (area 17 or V1) show clear orientation selectivity, unlike those of the lateral geniculate nucleus (LGN) cells which provide their visual input. The intrinsic circuitry of V1 cells is believed to be partly responsible for this selectivity. We investigated the influence of ascending projections from neurons in the lower layers (5 and 6) of V1 on the orientation selectivity of single neurons in the upper layers (2, 3, and 4) by reversibly inactivating (“blocking”) lower layer neural activity with iontophoretic application of γ-aminobutyric acid (GABA) while recording from upper layer cells in the prosimian primate, Galago crassicaudatus. During lower layer blocking, the majority (20/28 = 71.4%) of upper layer neurons exhibited a change in the orientation of their preferred stimulus, a reduction in their orientation tuning, and/or an increase in their response amplitude. Twelve (42.9%) neurons exhibited shifts in their preferred orientation averaging 11 (±4) deg. These neurons were located, on average, 272 (±120) μm tangential from the vertical axis of the pipette center. Eleven neurons (39.2%) exhibited an average reduced orientation tuning of 52.5%. Their average location was 230 ± (115) ftm away from the vertical axis of the pipette. Five (17.9%) neurons with average location 145 (±75) firn from the vertical axis exhibited both effects. Two (7.1%) neurons that exhibited significant increases in response amplitude to stimulus angles within 10 deg of the peak excitatory stimulus without changes in orientation selectivity or tuning were located less than 100 μm from the vertical axis. The effects on the orientation tuning of cells were restricted in all cases to within ±30 deg of the preferred stimulus orientation. This suggests that layer blocking affects cells with preferred stimulus orientations similar to those of the recorded neurons. Only cells located within 500 μm tangential to the vertical axis of the injection site exhibited these effects. These results suggest that cells within layers 5 and 6 provide organized, orientation-tuned inhibition that sharpens the orientation tuning of cells in the upper cortical layers within the same, or closely neighboring, cell columns.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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