Neural correlates of crowding in macaque area V4

Abstract

Visual crowding refers to the phenomenon where a target object that is easily identifiable in isolation becomes difficult to recognize when surrounded by other stimuli (distractors). Extensive psychophysical studies support two alternative possibilities for the underlying mechanisms. One hypothesis suggests that crowding results from the loss of visual information due to pooled encoding of multiple nearby stimuli in the mid-level processing stages along the ventral visual pathway. Alternatively, crowding may arise from limited resolution in decoding object information during recognition and the encoded information may remain inaccessible unless it is salient. To rigorously test these alternatives, we studied the responses of single neurons in macaque area V4, an intermediate stage of the ventral, object-processing pathway, to parametrically designed crowded displays and their texture-statistics matched metameric counterparts. Our investigations reveal striking parallels between how crowding parameters, e.g., number, distance, and position of distractors, influence human psychophysical performance and V4 shape selectivity. Importantly, we found that enhancing the salience of a target stimulus could reverse crowding effects even in highly cluttered scenes and such reversals could be protracted reflecting a dynamical process. Overall, we conclude that a pooled encoding of nearby stimuli cannot explain the observed responses and we propose an alternative model where V4 neurons preferentially encode salient stimuli in crowded displays. Significance StatementPsychophysicists have long studied the phenomena of visual crowding, but the underlying neural mechanisms are unknown. Our results reveal striking correlations between the responses of neurons in mid-level visual cortical area V4 and psychophysical demonstrations, revealing that crowding is influenced not only by the number and spatial arrangement of distractors but also by the similarity of features between target and distractors, as well as among the distractors themselves. Overall, our studies provide strong evidence that the visual system uses strategies to preferentially encode salient features in a visual scene presumably to process visual information efficiently. When multiple nearby stimuli are equally salient, the phenomenon of crowding ensues.