Partial information decomposition reveals that synergistic neural integration is greater downstream of recurrent information flow in organotypic cortical cultures

PLoS Comput Biol. 2021 Jul 12;17(7):e1009196. doi: 10.1371/journal.pcbi.1009196. eCollection 2021 Jul.

Abstract

The directionality of network information flow dictates how networks process information. A central component of information processing in both biological and artificial neural networks is their ability to perform synergistic integration-a type of computation. We established previously that synergistic integration varies directly with the strength of feedforward information flow. However, the relationships between both recurrent and feedback information flow and synergistic integration remain unknown. To address this, we analyzed the spiking activity of hundreds of neurons in organotypic cultures of mouse cortex. We asked how empirically observed synergistic integration-determined from partial information decomposition-varied with local functional network structure that was categorized into motifs with varying recurrent and feedback information flow. We found that synergistic integration was elevated in motifs with greater recurrent information flow beyond that expected from the local feedforward information flow. Feedback information flow was interrelated with feedforward information flow and was associated with decreased synergistic integration. Our results indicate that synergistic integration is distinctly influenced by the directionality of local information flow.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Computational Biology
  • Feedback, Physiological
  • Mice
  • Models, Neurological*
  • Nerve Net / physiology*
  • Neural Networks, Computer*
  • Neurons / physiology
  • Organ Culture Techniques
  • Somatosensory Cortex / physiology*
  • Synaptic Transmission / physiology

Grants and funding

ELN was supported by a grant from the Whitehall Foundation (17-12-114). JMB was supported by grants from the National Science Foundation (1429500, 1513779). This research was supported in part by Lilly Endowment, Inc., through its support for the Indiana University Pervasive Technology Institute. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.