Beyond Freezing: Temporal Expectancy of an Aversive Event Engages the Amygdalo–Prefronto–Dorsostriatal Network

Abstract

Abstract During Pavlovian aversive conditioning, a neutral conditioned stimulus (CS) becomes predictive of the time of arrival of an aversive unconditioned stimulus (US). Using a paradigm where animals had to discriminate between a CS+ (associated with a footshock) and a CS− (never associated with a footshock), we show that, early in training, dynamics of neuronal oscillations in an amygdalo–prefronto–striatal network are modified during the CS+ in a manner related to the CS–US time interval (30 or 10 s). This is the case despite a generalized high level of freezing to both CS+ and CS−. The local field potential oscillatory power was decreased between 12 and 30 Hz in the dorsomedial striatum (DMS) and increased between 55 and 95 Hz in the prelimbic cortex (PL), while the coherence between DMS, PL, and the basolateral amygdala was increased in the 3–6 Hz frequency range up to the expected time of US arrival only for the CS+ and not for the CS−. Changing the CS–US interval from 30 to 10 s shifted these changes in activity toward the newly learned duration. The results suggest a functional role of the amygdalo–prefronto–dorsostriatal network in encoding temporal information of Pavlovian associations independently of the behavioral output.