Noisy Spiking in Visual Area V2 of Amblyopic Monkeys

Interocular decorrelation of input signals in developing visual cortex can cause impaired binocular vision and amblyopia. While increased ‘intrinsic noise9 is thought to be responsible for a range of perceptual deficits in amblyopic humans, the neural basis for the elevated perceptual noise in amblyopic primates is not known. Here we tested the idea that perceptual noise is linked to the neuronal spiking noise (variability) resulting from developmental alterations in cortical circuitry. To assess spiking noise, we analyzed: the contrast dependent dynamics of spike counts and spiking irregularity by calculating the square of the coefficient of variation in inter spike intervals (CV 2 ) and the trial-to-trial fluctuations in spiking (m-FF) in visual area V2 of monkeys reared with chronic monocular defocus. In ‘amblyopic9 neurons, the contrast vs. response functions and the spike count dynamics exhibited significant deviations from comparable data for normal monkeys. Spiking irregularity (CV 2 ) was pronounced in amblyopic neurons for high contrast stimuli. The trial-to-trial variability in spiking (m-FF) was abnormally high in amblyopic neurons for low contrast gratings. The spike count, CV 2 , and m-FF of spontaneous activity were also elevated in amblyopic neurons. These contrast-dependent spiking irregularities were correlated with the level of binocular suppression in these V2 neurons and with the severity of perceptual loss for individual monkeys. Our results suggest that the developmental alterations in ‘normalization9 mechanisms, resulting from early binocular suppression, can explain much of these contrast-dependent spiking abnormalities in V2 neurons and the perceptual performance of our amblyopic monkeys. SIGNIFICANCE STATEMENT Amblyopia is a common developmental vision disorder in humans. Despite the extensive animal studies on how amblyopia emerges, we know surprisingly little about the neural basis of amblyopia in humans and non-human primates. While the vision of amblyopic humans is often described as being ‘noisy9 by perceptual and modeling studies, the exact nature or origin of this elevated perceptual noise is not known. We show that elevated and noisy spontaneous activity and contrast-dependent ‘noisy spiking9 (spiking irregularity and trial-to-trail fluctuations in spiking) in neurons of visual area (V2) could limit the visual performance of amblyopic primates. Moreover we discovered that the noisy spiking is linked to a high level of binocular suppression in visual cortex during development.