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Dynamics of orientation tuning in macaque primary visual cortex

Abstract

Orientation tuning of neurons is one of the chief emergent characteristics of the primary visual cortex, VI (refs 1,2). Neurons of the lateral geniculate nucleus, which comprise the thalamic input to VI, are not orientation-tuned, but the majority of VI neurons are quite selective. How orientation tuning arises within VI is still controversial1,3–17. To study this problem, we measured how the orientation tuning of neurons evolves with time18–20 using a new method: reverse correlation in the orientation domain. Orientation tuning develops after a delay of 30–45 milliseconds and persists for 40–85 ms. Neurons in layers 4Cα or 4Cβ, which receive direct input from the thalamus, show a single orientation preference which remains unchanged throughout the response period. In contrast, the preferred orientations of output layer neurons (in layers 2,3,4B, 5 or 6) usually change with time, and in many cases the orientation tuning may have more than one peak. This difference in dynamics is accompanied by a change in the sharpness of orientation tuning; cells in the input layers are more broadly tuned than cells in the output layers. Many of these observed properties of output layer neurons cannot be explained by simple feedforward models1,3–6, whereas they arise naturally in feedback networks7–17. Our results indicate that VI is more than a bank of static oriented filters; the dynamics of output layer cells appear to be shaped by intracortical feedback.

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Ringach, D., Hawken, M. & Shapley, R. Dynamics of orientation tuning in macaque primary visual cortex. Nature 387, 281–284 (1997). https://doi.org/10.1038/387281a0

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