A synaptic mechanisms for encoding the learned value of action-derived safety

Mario Penzo, PhD
Chief
Section on the Neural Circuits of Emotion and Motivation
National Institute of Mental Health

Adaptive behavior requires that behaviorally relevant signals gain access to neural circuits that guide action. The thalamus has long been proposed to regulate information flow to cortical and subcortical systems, yet whether it also tracks internally generated goal signals remains unclear. Here, we show that neurons in the paraventricular thalamus (PVT) projecting to the nucleus accumbens (NAc) encode the motivational value of safety during active avoidance. As mice learn to avoid threat, PVT→NAc neurons develop a signal that emerges selectively at successful avoidance, is experience-dependent, and diminishes following outcome devaluation. Selective silencing of the PVT→NAc pathway at safety onset selectively reduces the motivational value assigned to safety without impairing action–outcome learning. Mechanistically, PVT input engages cholinergic interneurons in the NAc to regulate dopamine release via synaptic potentiation mediated by GluA2-lacking AMPA receptors at PVT–CIN synapses. Disrupting this plasticity selectively reduces the motivational impact of safety. These findings identify a thalamostriatal mechanism through which learned goals gain stable access to motivational circuitry.