Interneuronal correlations dynamically adjust to task demands at multiple time-scales

Abstract

Functional neuronal correlations between pairs of neurons are thought to play an important role in neuronal information processing and optimal neuronal computations during attention, perception, decision-making and learning. Here, we report dynamic changes in prefrontal neuronal noise correlations at multiple time-scales, as a function of task contingencies. Specifically, we record neuronal activity from the macaque frontal eye fields, a cortical region at the source of spatial attention top-down control, while the animals are engaged in tasks of varying cognitive demands. We show that the higher the task demand and cognitive engagement the lower noise correlations. We further report that within a given task, noise correlations significantly decrease in epoch of higher response probability. Last we show that the power of the rhythmic modulations of noise correlations in the alpha and beta frequency ranges also decreases in the most demanding tasks. All of these changes in noise correlations are associated with layer specific modulations in spikes-LFP phase coupling, suggesting both a long-range and a local intra-areal origin. Over all, this indicates a highly dynamic adjustment of noise correlations to ongoing task requirements and suggests a strong functional role of noise correlations in cognitive flexibility. Significance statement Cortical neurons are densely interconnected. As a result, pairs of neurons share some degree of variability in their neuronal responses. This impacts how much information is present within a neuronal population and is critical to attention, decision-making and learning. Here we show that, in the prefrontal cortex, this shared inter-neuronal variability is highly flexible, decreasing across tasks as cognitive demands increase and within trials in epochs of maximal behavioral demand. It also fluctuates in time at a specific rhythm, the power of which decreases for higher cognitive demand. All of these changes in noise correlations are associated with layer specific modulations in spikes-LFP phase coupling. Over all, this suggests a strong functional role of noise correlations in cognitive flexibility.