Global organization of neuronal activity only requires unstructured local connectivity

Elife. 2022 Jan 20:11:e68422. doi: 10.7554/eLife.68422.

Abstract

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.

Keywords: balanced state; beyond-mean-field theory; correlated activity; long-range coordination; motor cortex; neuroscience; reach-to-grasp task; rhesus macaque.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • Electrophysiology
  • Female
  • Macaca mulatta
  • Male
  • Models, Neurological*
  • Motor Cortex* / cytology
  • Motor Cortex* / physiology
  • Nerve Net* / cytology
  • Nerve Net* / physiology
  • Neurons* / cytology
  • Neurons* / physiology

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.