Altered functional interactions between neurons in primary visual cortex of macaque monkeys with experimental amblyopia

Abstract

Amblyopia, a disorder in which vision through one of the eyes is degraded, arises because of defective processing of information by the visual system. Amblyopia often develops in humans after early misalignment of the eyes (strabismus) and can be simulated in macaque monkeys by artificially inducing strabismus. In such amblyopic animals, single-unit responses in primary visual cortex (V1) are appreciably reduced when evoked by the amblyopic eye compared with the other (fellow) eye. However, this degradation in single V1 neuron responsivity is not commensurate with the marked losses in visual sensitivity and resolution measured behaviorally. Here we explored the idea that changes in patterns of coordinated activity across populations of V1 neurons may contribute to degraded visual representations in amblyopia, potentially making it more difficult to read out evoked activity to support perceptual decisions. We studied the visually evoked activity of V1 neuronal populations in three macaques ( Macaca nemestrina) with strabismic amblyopia and in one control animal. Activity driven through the amblyopic eye was diminished, and these responses also showed more interneuronal correlation at all stimulus contrasts than responses driven through the fellow eye or responses in the control animal. A decoding analysis showed that responses driven through the amblyopic eye carried less visual information than other responses. Our results suggest that part of the reduced visual capacity of amblyopes may be due to changes in the patterns of functional interaction among neurons in V1. NEW & NOTEWORTHY Previous work on the neurophysiological basis of amblyopia has largely focused on relating behavioral deficits to changes in visual processing by single neurons in visual cortex. In this study, we recorded simultaneously from populations of primary visual cortical (V1) neurons in macaques with amblyopia. We found changes in the strength and pattern of shared response variability between neurons. These changes in neuronal interactions could impair the visual representations of V1 populations driven by the amblyopic eye.