Contrast Adaptation Contributes to Contrast-Invariance of Orientation Tuning of Primate V1 Cells

Lionel G Nowak,Pascal Barone

doi:10.1371/journal.pone.0004781

Lionel G Nowak, Pascal Barone

Open Access

https://doi.org/10.1371/journal.pone.0004781

Copy DOI

Abstract

BackgroundStudies in rodents and carnivores have shown that orientation tuning width of single neurons does not change when stimulus contrast is modified. However, in these studies, stimuli were presented for a relatively long duration (e. g., 4 seconds), making it possible that contrast adaptation contributed to contrast-invariance of orientation tuning. Our first purpose was to determine, in marmoset area V1, whether orientation tuning is still contrast-invariant with the stimulation duration is comparable to that of a visual fixation.Methodology/Principal FindingsWe performed extracellular recordings and examined orientation tuning of single-units using static sine-wave gratings that were flashed for 200 msec. Sixteen orientations and three contrast levels, representing low, medium and high values in the range of effective contrasts for each neuron, were randomly intermixed. Contrast adaptation being a slow phenomenon, cells did not have enough time to adapt to each contrast individually. With this stimulation protocol, we found that the tuning width obtained at intermediate contrast was reduced to 89% (median), and that at low contrast to 76%, of that obtained at high contrast. Therefore, when probed with briefly flashed stimuli, orientation tuning is not contrast-invariant in marmoset V1. Our second purpose was to determine whether contrast adaptation contributes to contrast-invariance of orientation tuning. Stationary gratings were presented, as previously, for 200 msec with randomly varying orientations, but the contrast was kept constant within stimulation blocks lasting >20 sec, allowing for adaptation to the single contrast in use. In these conditions, tuning widths obtained at low contrast were still significantly less than at high contrast (median 85%). However, tuning widths obtained with medium and high contrast stimuli no longer differed significantly.Conclusions/SignificanceOrientation tuning does not appear to be contrast-invariant when briefly flashed stimuli vary in both contrast and orientation, but contrast adaptation partially restores contrast-invariance of orientation tuning.

Highlights

For most neurons in area V1, response amplitude depends on stimulus orientation [e.g., 1,2]
It was designed to tease apart the effects of contrast from those of contrast adaptation on orientation tuning, while at the same time providing the possibility to examine orientation tuning for a stimulation duration comparable to that of a visual fixation
We examined whether the effects of contrast on orientation tuning width and relative untuned response amplitude’’ (RURA) differed between layers

Summary

Introduction

For most neurons in area V1, response amplitude depends on stimulus orientation [e.g., 1,2]. Following Sclar and Freeman (1982) [6], multiple studies have examined interactions between contrast and orientation selectivity [7,8,9,10,11,12,13] All these studies demonstrated that, response amplitude increases with contrast, the width of orientation-tuning curves remains constant. Studies in rodents and carnivores have shown that orientation tuning width of single neurons does not change when stimulus contrast is modified. In these studies, stimuli were presented for a relatively long duration Our first purpose was to determine, in marmoset area V1, whether orientation tuning is still contrast-invariant with the stimulation duration is comparable to that of a visual fixation

Objectives

Methods

Results

Conclusion