Flexible modulation of neuronal population dynamics drives variable decision-making in C. elegans

Abstract

Behavior arises from the interplay between spontaneous brain dynamics and sensory-driven responses, yet how spontaneous neural activity shapes variability in decision-making remains unclear. We leverage the tractable C. elegans nervous system to address this question. During oxygen avoidance, we observe binary trial-to-trial variability in behavioral responses. Whole-brain calcium imaging reveals a brain-wide sensory-to-motor transformation in which sensory neurons faithfully encode the stimulus but do not predict choice. Instead, decision-related information is distributed across interneurons and motor neurons, encoded through a neuronal subspace. This decision-biasing state evolves slowly during the pre-stimulus period, resembling preparatory dynamics for spontaneous behavioral transitions but receives neuromodulatory contributions. Optogenetic manipulations reveal that only a subset of neurons within this distributed representation are causally connected to choice. This reveals a dissociation between broad information sharing and control via dedicated localized nodes. Thus, response variability arises from slowly evolving modulation of brain states rather than stochastic circuit noise.