Amygdala central nucleus interacts with dorsolateral striatum to regulate the acquisition of habits

• Published in: The Journal of neuroscience Vol. 32; no. 3; pp. 1073 - 1081
• Main Authors: Lingawi, Nura W, Balleine, Bernard W
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 18.01.2012
• Subjects: Amygdala - injuries; Amygdala - metabolism; Amygdala - physiology; Analysis of Variance; Animals; Conditioning, Classical - physiology; Conditioning, Operant - drug effects; Conditioning, Operant - physiology; Corpus Striatum - pathology; Denervation - methods; Eating; Extinction, Psychological; Food Deprivation - physiology; Food Preferences - drug effects; Food Preferences - physiology; Glial Fibrillary Acidic Protein - metabolism; Habits; Ibotenic Acid - toxicity; Male; Myelin Sheath - metabolism; Rats; Rats, Long-Evans; Sucrose - administration & dosage; Transfer (Psychology)
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.4806-11.2012

The role of the amygdala central nucleus (CeN) in habit learning was assessed in two experiments. First, we examined the effects of bilateral lesions of the anterior CeN on an overtraining-induced lever press habit evaluated using an outcome devaluation protocol. Overtraining generated habitual performance and rendered sham lesioned rats insensitive to outcome devaluation, an effect that was also found in rats given control lesions of the posterior CeN. In contrast, rats with lesions of the anterior CeN did not show normal habit acquisition and their performance remained goal-directed and sensitive to outcome devaluation. Nevertheless, lesions of either the posterior or the anterior CeN abolished the general excitatory influence of a Pavlovian conditioned stimulus on instrumental performance. Second, we assessed the functional interaction between the CeN and dorsolateral striatum (DLS), a region previously implicated in the acquisition of habits, using asymmetrical lesions to disconnect these structures. Rats were given a unilateral lesion of anterior CeN and a unilateral lesion of the DLS, made either ipsilateral (control) or contralateral (disconnection) to the CeN lesion, and given overtraining followed by outcome devaluation. Although the ipsilateral lesioned rats were insensitive to devaluation, the contralateral CeN-DLS lesion impaired habit acquisition, rendering performance sensitive to the devaluation treatment. These results are the first to implicate the CeN and its connection with a circuit involving DLS in habit learning. They imply that, in instrumental conditioning, regions of amygdala parse the instrumental outcome into the reward and reinforcement signals mediating goal-directed and habitual actions, respectively.