Mixed selectivity coding of sensory and motor social signals in the thalamus of a weakly electric fish

Abstract

High-level neural activity often exhibits mixed selectivity to multivariate signals. How such representations arise and modulate natural behavior is poorly understood. We addressed this question in weakly electric fish, whose social behavior is relatively low dimensional and can be easily reproduced in the laboratory. We report that the preglomerular complex, a thalamic region exclusively connecting midbrain with pallium, implements a mixed selectivity strategy to encode interactions related to courtship and rivalry. We discuss how this code enables the pallial recurrent networks to control social behavior, including dominance in male-male competition and female mate selection. Notably, response latency analysis and computational modeling suggest that corollary discharge from premotor regions is implicated in flagging outgoing communications and thereby disambiguating self- versus non-self-generated signals. These findings provide new insights into the neural substrates of social behavior, multi-dimensional neural representation, and its role in perception and decision making.

Keywords: aggression; combinatorial coding; communication; corollary discharge; courtship; electric fish; mixed selectivity; rivalry; social behavior; thalamus.