Nonmonotonic spatial structure of interneuronal correlations in prefrontal microcircuits

Significance The spatial structure of correlated activity of neurons in lower-order visual areas has been shown to linearly decrease as a measure of distance. The shape of correlated variability is a defining feature of cortical microcircuits, as it constrains the computational power and diversity of a region. We show here a nonmonotonic spatial structure of functional connectivity in the prefrontal cortex (PFC) where distal interactions are just as strong as proximal interactions during visual engagement of functionally similar PFC neurons. Such a nonmonotonic structure of functional connectivity could have far-reaching consequences in rethinking the nature and role of prefrontal microcircuits in various cognitive states. Correlated fluctuations of single neuron discharges, on a mesoscopic scale, decrease as a function of lateral distance in early sensory cortices, reflecting a rapid spatial decay of lateral connection probability and excitation. However, spatial periodicities in horizontal connectivity and associational input as well as an enhanced probability of lateral excitatory connections in the association cortex could theoretically result in nonmonotonic correlation structures. Here, we show such a spatially nonmonotonic correlation structure, characterized by significantly positive long-range correlations, in the inferior convexity of the macaque prefrontal cortex. This functional connectivity kernel was more pronounced during wakefulness than anesthesia and could be largely attributed to the spatial pattern of correlated variability between functionally similar neurons during structured visual stimulation. These results suggest that the spatial decay of lateral functional connectivity is not a common organizational principle of neocortical microcircuits. A nonmonotonic correlation structure could reflect a critical topological feature of prefrontal microcircuits, facilitating their role in integrative processes.

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