Chromatic detection from cone photoreceptors to individual V1 neurons to behavior in macaque monkeys

Abstract

Vision is the culmination of countless biophysical events from the initial stages of sensory transduction to conscious perception. Despite the complexity of this process, our brains encode the visual world effortlessly in only a few hundred milliseconds. Color is a particularly salient visual cue yet we know relatively little about how color is encoded by neurons in the neocortex. Using a combination of neurophysiological, psychophysical, and theoretical approaches we investigated the role of neurons in the primary visual cortex (V1) in chromatic contrast detection in macaque monkeys. We recorded extracellularly from individual V1 neurons and tested the hypothesis that V1 neurons behave as the linear cardinal mechanisms at the observer's detection threshold. Although many neurons in V1 were active at detection threshold, we found that their responses were inconsistent with the cardinal mechanisms model. A subset of these neurons were responsive to both cardinal colors at detection threshold indicating that some V1 neurons are very broadly tuned to color even in response to low-contrast stimuli. Next, we investigated two sources of noise that affect the detectability of chromatic stimuli: eye-movements and noise in the phototransduction cascade. Monkeys made low amplitude (<1º) saccades (microsaccades) while performing a detection task that suppressed their ability to see low spatial frequency achromatic (but not red-green isoluminant) stimuli. An analysis of saccade-triggered responses revealed that cone-opponent and non-opponent V1 neurons are both modulated by microsaccades, suggesting the the locus of the differential behavioral effect on achromatic and isoluminant stimuli is downstream of V1. Lastly, we created a model of stimulus transduction in the cone outer segments to compare the sensitivity of individual V1 neurons and behaving monkeys to the limits imposed by phototransduction in the cones. We found that the temporal frequency dependence of the monkey's contrast sensitivity to red-green isoluminant (but not luminance) followed closely the frequency dependence of signal processing in the cones. The shape of the temporal contrast sensitivity function can be explained almost entirely by the deterministic component of the modeled cone responses; noise in the phototransduction cascade made only minor contributions.