Simultaneous silence organizes structured higher-order interactions in neural populations.
Activity patterns of neural population are constrained by underlying biological mechanisms. These patterns are characterized not only by individual activity rates and pairwise correlations but also by statistical dependencies among groups of neurons larger than two, known as higher-order interactions (HOIs). While HOIs are ubiquitous in neural activity, primary characteristics of HOIs remain unknown. Here, we report that simultaneous silence (SS) of neurons concisely summarizes neural HOIs. Spontaneously active neurons in cultured hippocampal slices express SS that is more frequent than predicted by their individual activity rates and pairwise correlations. The SS explains structured HOIs seen in the data, namely, alternating signs at successive interaction orders. Inhibitory neurons are necessary to maintain significant SS. The structured HOIs predicted by SS were observed in a simple neural population model characterized by spiking nonlinearity and correlated input. These results suggest that SS is a ubiquitous feature of HOIs that constrain neural activity patterns and can influence information processing.
RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan.
Hideaki
H
Shimazaki
Commonwealth Computer Research Inc., 1422 Sachem Pl., Unit #1, Charlottesville, VA 22901, U.S.A.
Kolia
K
Sadeghi
Graduate School of Pharmaceutical Sciences, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
Tomoe
T
Ishikawa
1] Graduate School of Pharmaceutical Sciences, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan [2] Heart to Heart Science, Center for Information and Neural Networks, 1-4 Yamadaoka, Suita, Osaka, 565-0871, Japan.
Yuji
Y
Ikegaya
1] RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan [2] Department of Computational Intelligence and Systems Science, Tokyo Institute of Technology, Yokohama 226-8502, Japan.
Taro
T
Toyoizumi
D000818:Animals; D005260:Female; D006624:Hippocampus / Q000502:physiology; D008297:Male; D008959:Models, Neurological; D009415:Nerve Net / Q000502:physiology*; D009474:Neurons / Q000502:physiology*; D051381:Rats; D017208:Rats, Wistar