Crowding alters feature encoding in macaque visual cortex

Abstract:

We are good at judging the visual features of objects in peripheral vision when they are viewed in isolation. However, when these same objects are surrounded by adjacent stimuli in the visual field, local feature discrimination is often impaired. This phenomenon, known as visual crowding, has been extensively studied at the behavioral level in humans, revealing many factors that affect local feature perception. In contrast, little is known at a mechanistic level about how crowding affects the activity of single neurons or populations of neurons at distinct stages of the visual system, which together ultimately give rise to these altered sensory percepts. We studied crowding behaviorally and neurophysiologically in macaque monkeys, an excellent animal model of the human visual system. Animals were trained to perform a fine orientation discrimination task for peripheral targets. Overall, monkeys exhibited strong perceptual crowding; effect size and error patterns were similar to those of human observers.

We then asked how crowding altered the representation of target orientation in neuronal populations at the first stage of cortical processing, primary visual cortex (V1). Crowding stimuli strongly modulated the average firing rate of individual V1 neurons, suppressing most but facilitating others, which resulted in changes of the tuning curves for target orientation. In addition, crowding produced modest but significant changes in both individual neuronal variability (Fano factor) and shared variability (pairwise spike count correlation). At the V1 population level, this resulted in moderate information losses in encoded target orientation under crowding, and was driven largely by the varied change in average neuronal firing rates. We show that both increases and decreases in overall firing under crowding can result in losses of feature information, provided these modulations are of the right form. The extent to which changes in V1 populations under crowding limit local feature perception will depend on how these signals are read out and integrated in downstream cortical circuits. Our results show that the effects of crowding in peripheral vision are already evident in the first stages of cortical processing.