Mixed Representations of Sound and Action in the Auditory Midbrain

Abstract

Linking sensory input and its consequences is a fundamental brain operation. During behavior, neural activity of neo-cortical and limbic systems often reflects dynamic combinations of sensory and task-dependent variables, and these “mixed representations” are suggested to be important for perception, learning, and plasticity. However, the extent to which such integrative computations might occur outside of the forebrain is less clear. Here, we conduct cellular-resolution 2-photon Ca2+imaging in the superficial “shell” layers of the inferior colliculus (IC), as head-fixed mice of either sex perform a reward-based psychometric auditory task. We find that the activity of individual shell IC neurons jointly reflects auditory cues, mice’s actions, and behavioral trial outcomes, such that trajectories of neural population activity diverge depending on mice’s behavioral choice. Consequently, simple classifier models trained on shell IC neuron activity can predict trial-by-trial outcomes, even when training data are restricted to neural activity occurring prior to mice’s instrumental actions. Thus, in behaving mice, auditory midbrain neurons transmit a population code that reflects a joint representation of sound, actions, and task-dependent variables.Significance StatementNeurons in IC’s superficial “shell” layers preferentially project to higher-order thalamic nuclei that are strongly activated by sounds and their consequences, thereby combining sensory and task dependent information. This sensory-behavior integration is thought critical for a variety of behaviorally relevant functions, such as establishing learned sound valence. However, whether such “mixed representations” reflect unique properties of thalamocortical networks, or rather are present in other areas, is unclear. We show that in behaving mice, many shell IC neurons are modulated by sounds and mice’s actions. Consequently, shell IC population activity suffices to predict trial outcomes prior to the rewarded action. Our data thus establish shell IC nuclei as a novel locus of behaviorally relevant mixed representations.