Synchronous Rhythmic Activity in Area V4 Can Impair Shape Detection and Neuronal Reliability

Abstract

Rhythms at a population level are a defining characteristic of both normal and pathological cortical activities, but it is unclear how such rhythms interact with the activity of specific neurons to impact task performance on a trial-by-trial basis. We address this by employing a challenging visual detection task in which male rhesus macaques must signal the presentation of a shape embedded in a noisy background. We analyzed the rhythmic activity in the local field potential (LFP) and single neuron activity in area V4, a brain area strongly implicated in shape perception, prior to such presentations and focused on two different frequency ranges: alpha/beta (10–30 Hz), in which coherence was particularly strong and spatially extensive, and gamma (50–70 Hz), which has traditionally been strongly associated with single unit activity. We find that within sessions, there were periods of time during which successful detection was associated with the absence of rhythmic activity prior to shape presentation in either frequency range. During these periods, rhythmic quiescence prior to shape presentation could predict whether the shape would be detected by the animal with high accuracy. Importantly, for both frequency ranges, the individual neurons carrying the most relevant information with regard to the task had the weakest coupling to LFP rhythms. These results are consistent with spatially distributed rhythmic activity acting as a source of decision noise in the context of rapid visual detection by reducing the moment-to-moment reliability of task-relevant information carried by individual neurons.