Instrumental Punishment Learning Enhances the Intrinsic Excitability of Basolateral Amygdala Neurons
Eddie T Wise, Philip Jean-Richard-dit-BresseliD, Joanna Oi-Yue YauiD, Gavan P. McNallyiD, John PoweriD
Abstract
The basolateral amygdala (BLA) is a structure that is critical for forming Pavlovian and instrumental emotional associations. Previous studies have established that Pavlovian fear conditioning increases the intrinsic excitability of BLA projection neurons. Learning-associated increases in excitability are hypothesised to facilitate the induction of synaptic plasticity and integration of neurons into functional learning circuits. Here, we examined whether instrumental learning produces similar changes in intrinsic excitability. Male and Female Long Evans rats were trained to lever press for a food reward and subsequently split into 3 behavioural groups; punished, yoked, and reward. Punished rats received response-contingent footshocks, yoked rats received response-independent footshocks, and reward rats received no shock. Intrinsic excitability was measured as the number of action potentials (APs) evoked by a series of depolarising current injections during whole-cell patch clamp recordings. Reward learning increased the intrinsic excitability of BLA projection neurons compared to naive controls. Punishment training maintained excitability and excitability was correlated with performance on the punishment task. Response-independent footshocks arrested reward-associated increases in excitability, reverting the BLA neurons to a naive state. Group differences were observed in AP half-width and the current underlying the post-burst AHP. Together, these findings show that instrumental reward learning enhances the intrinsic excitability of BLA projection neurons, potentially supporting action-outcome encoding by promoting synaptic plasticity and circuit integration. The results also suggest that different forms of learning engage distinct biophysical adaptations. A mechanistic understanding of the neurobiology underlying instrumental association learning may help inform the development of treatments for psychiatric disorders characterized by deficits in this process, such as major depressive disorder and conduct disorder.
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