Rhythmic variations in prefrontal inter-neuronal correlations, their underlying mechanisms and their behavioral correlates

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. These noise correlations are often assumed to be stable in time. However, recent studies suggest that cognitive processes are rhythmic, this rhythmicity accounting for variations in overt behavioral performance. Whether this rhythmicity coincides with variations in shared noise variability is unknown. Here, we perform simultaneous recordings from the macaque frontal eye fields, while animals are engaged in a spatial memory task. We report that noise correlations in prefrontal cortex fluctuate rhythmically in the high alpha (10-16Hz) and beta (20-30Hz) frequency ranges. Importantly, these rhythmic modulations in shared neuronal variability account for dynamic changes in overt behavioral performance. They also coincide with increased spike-LFP phase coupling in these specific frequency ranges, the spatial profile of which vary between superficial and deep cortical layers. Finally, we demonstrate, using an artificial neuronal model, that rhythmic variations in noise correlation oscillations parsimoniously arise from long range (LFP) and local spike-LFP phase coupling mechanisms. Thus a significant portion of noise correlation fluctuations can be attributed to long-range global network rhythmicity.