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The Journal of Neuroscience, March 16, 2005, 25(11):2771-2780; doi:10.1523/JNEUROSCI.3894-04.2005

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Behavioral/Systems/Cognitive
Lesion to the Nigrostriatal Dopamine System Disrupts Stimulus-Response Habit Formation

Alexis Faure,¹ Ulrike Haberland,¹ Françoise Condé,² and Nicole El Massioui¹

¹Laboratoire de Neurobiologie de l'Apprentissage, de la Mémoire et de la Communication, Unité Mixte de Recherche 8620, Université Paris Sud, 91405 Orsay Cedex, France, and ²Unité de Recherche Associée 2210, Commissariat à l'Energie Atomique, Centre National de Recherche Scientifique, Service Hospitalier Frédéric Joliot, 91401 Orsay Cedex, France

Acquisition and performance of instrumental actions are assumed to require both action-outcome and stimulus-response (S-R) habit processes. Over the course of extended training, control over instrumental performance shifts from goal-directed action-outcome associations to S-R associations that progressively gain domination over behavior. Lesions of the lateral part of the dorsal striatum disrupt this process, and rats with lesions to the lateral striatum showed selective sensitivity to devaluation of the instrumental outcome (Yin et al., 2004), indicating that this area is necessary for habit formation. The present experiment further explored the basis of this dysfunction by examining the ability of rats subjected to bilateral 6-hydroxydopamine lesions of the nigrostriatal dopaminergic pathway to develop behavioral autonomy with overtraining. Rats were given extended training on two cued instrumental tasks associating a stimulus (a tone or a light) with an instrumental action (lever press or chain pull) and a food reward (pellets or sucrose). Both tasks were run daily in separate sessions. Overtraining was followed by a test of goal sensitivity by satiety-specific devaluation of the reward. In control animals, one action (lever press) was insensitive to reward devaluation, indicating that it became a habit, whereas the second action (chain pull) was still sensitive to goal devaluation. This result provides evidence that the development of habit learning may depend on the characteristics of the response. In dopamine-depleted rats, lever press and chain pull remained sensitive to reward devaluation, evidencing a role of striatal dopamine transmission in habit formation.

Key words: lateral striatum; substantia nigra; dopamine; instrumental learning; habit formation; basal ganglia

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Received Sep 20, 2004; revised January 13, 2005; accepted January 18, 2005.

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