The Amygdalostriatal Transition Area Exhibits Lateral Amygdala-Like Spiking Activity and Tone-Shock Pairing-Induced...

During Pavlovian fear conditioning, presentation of a conditioned stimulus, such as a tone, together with an unconditioned stimulus, such as an electrical shock, excites neurons in the lateral amygdala (LA). Prevailing models propose that sensory stimulus-evoked activity in the LA is subsequently propagated to its downstream nuclei: the basal amygdala (BA) and central amygdala (CeA). To test this assumption, we performed in vivo electrophysiological recordings in awake, head-fixed male and female mice. We found that tone presentation did not elicit a significant increase in firing in BA or CeA neurons. In contrast, shock presentation evoked similarly robust spiking responses in LA and BA neurons but only a modest increase in CeA neurons. Notably, neurons in the amygdalostriatal transition area (AStria) exhibited LA-like sensory stimulus-evoked responses at both short (<25 ms) and longer (<500 ms) timescales. To examine the role of feedforward inhibition in tone- and shock-evoked activity, we investigated the contribution of parvalbumin interneurons using optogenetics and found that short-latency (<25 ms) spiking in both the LA and AStria was regulated by these inhibitory cells. Finally, LA and AStria neurons exhibited remarkably similar response types, spiking dynamics, and pairing-induced plasticity during repeated tone presentations, subsequent tone-shock pairings, and post-pairing tone presentations. Together, these findings support a model in which the LA and AStria operate in parallel, similarly integrating tone and shock signals during fear conditioning, whereas BA and CeA neurons are not robustly recruited by these sensory stimuli under the conditions tested.Significance Statement Prevailing models of conditioned fear learning state that sensory stimulus-evoked activity in the lateral amygdala (LA) is relayed to the basal (BA) and central (CeA) amygdala nuclei. Using in vivo recordings in awake, head-fixed mice, we find that BA and CeA neurons show no significant tone-evoked firing and only modest activation to the electrical shocks. In contrast, neurons in the amygdalostriatal transition area (AStria) closely mirror neuronal responses and spiking dynamics in LA, with sensory stimulus-evoked spiking controlled by parvalbumin interneurons. These findings identify circuits within the LA and AStria, rather than BA or CeA, as the neuronal networks processing sensory signals during Pavlovian fear conditioning, challenging canonical models of amygdala information flow.