Global organization of neuronal activity only requires unstructured local connectivity.

Modern electrophysiological recordings simultaneously capture single-unit spiking activities of hundreds of neurons spread across large cortical distances. Yet, this parallel activity is often confined to relatively low-dimensional manifolds. This implies strong coordination also among neurons that are most likely not even connected. Here, we combine in vivo recordings with network models and theory to characterize the nature of mesoscopic coordination patterns in macaque motor cortex and to expose their origin: We find that heterogeneity in local connectivity supports network states with complex long-range cooperation between neurons that arises from multi-synaptic, short-range connections. Our theory explains the experimentally observed spatial organization of covariances in resting state recordings as well as the behaviorally related modulation of covariance patterns during a reach-to-grasp task. The ubiquity of heterogeneity in local cortical circuits suggests that the brain uses the described mechanism to flexibly adapt neuronal coordination to momentary demands.

On the Complexity of Resting State Spiking Activity in Monkey Motor Cortex.

Resting state has been established as a classical paradigm of brain activity studies, mostly based on large-scale measurements such as functional magnetic resonance imaging or magneto- and electroencephalography. This term typically refers to a behavioral state characterized by the absence of any task or stimuli. The corresponding neuronal activity is often called idle or ongoing. Numerous modeling studies on spiking neural networks claim to mimic such idle states, but compare their results with task- or stimulus-driven experiments, or to results from experiments with anesthetized subjects. Both approaches might lead to misleading conclusions. To provide a proper basis for comparing physiological and simulated network dynamics, we characterize simultaneously recorded single neurons' spiking activity in monkey motor cortex at rest and show the differences from spontaneous and task- or stimulus-induced movement conditions. We also distinguish between rest with open eyes and sleepy rest with eyes closed. The resting state with open eyes shows a significantly higher dimensionality, reduced firing rates, and less balance between population level excitation and inhibition than behavior-related states.