Contents lists available at ScienceDirect Behavioural Brain Research journal homepage: www.elsevier.com/locate/bbr Research report Reward loss and the basolateral amygdala: A function in reward comparisons Katsuyoshi Kawasaki a , Iván Annicchiarico b , Amanda C. Glueck b , Ignacio Morón c , Mauricio R. Papini b, ⁎ a Department of Psychology, Hoshi University, 2-4-41 Ebara, Shinagawa, Tokyo 142-8501, Japan b Department of Psychology, Texas Christian University, Fort Worth, TX 76129, USA c Department of Psychobiology, and Research Center for Mind, Brain, and Behavior (CIMCYC), University of Granada, Faculty of Psychology, Campus Cartuja, 18071 Granada, Spain ARTICLE INFO Keywords: Basolateral amygdala Reward loss Reward devaluation Successive negative contrast Autoshaping Extinction Open field activity ABSTRACT The neural circuitry underlying behavior in reward loss situations is poorly understood. We considered two such situations: reward devaluation (from large to small rewards) and reward omission (from large rewards to no rewards). There is evidence that the central nucleus of the amygdala (CeA) plays a role in the negative emotion accompanying reward loss. However, little is known about the function of the basolateral nucleus (BLA) in reward loss. Two hypotheses of BLA function in reward loss, negative emotion and reward comparisons, were tested in an experiment involving pretraining excitotoxic BLA lesions followed by training in four tasks: consummatory successive negative contrast (cSNC), autoshaping (AS) acquisition and extinction, anticipatory negative contrast (ANC), and open field testing (OF). Cell counts in the BLA (but not in the CeA) were significantly lower in animals with lesions vs. shams. BLA lesions eliminated cSNC and ANC, and accelerated extinction of lever pressing in AS. BLA lesions had no effect on OF testing: higher activity in the periphery than in the central area. This pattern of results provides support for the hypothesis that BLA neurons are important for reward comparison. The three affected tasks (cSNC, ANC, and AS extinction) involve reward comparisons. However, ANC does not seem to involve negative emotions and it was affected, whereas OF activity is known to involve negative emotion, but it was not affected. It is hypothesized that a circuit involving the thalamus, insular cortex, and BLA is critically involved in the mechanism comparing current and expected rewards. 1. Introduction The role of the amygdala in reward processes was first suggested in the early 1960s by a series of intracranial stimulation experiments. Wurtz and Olds [54] reported that stimulation electrodes placed in the basolateral amygdala (BLA) region yielded mainly escape responses (i.e., rats learned to press a lever that ended weak electrical currents delivered to the region), whereas electrodes located in the central amygdala (CeA) region supported lever approach (i.e., rats learned to press a lever paired with a weak electrical current delivered to the region). Wurtz and Olds [54] (1963, p. 948) concluded that “the amygdaloid complex contains a ‘projection area’ for environmental rewards and punishments,” with the BLA region involved in negative reinforcement and the CeA region in positive reinforcement. Whereas some subsequent results are consistent with this view (e.g., [24,40], the emerging picture of BLA's function includes a role in behavior main- tained by rewards. For example, infusion of the GABA A receptor antagonist muscimol into the BLA region suppressed lever pressing for food, without affecting the consumption of freely available food [51]. Thus, BLA inactivation seemed to affect appetitive (anticipatory) behavior, but not consummatory behavior. Moreover, Hatfield et al. [21] reported that whereas lesions of the BLA region did not affect simple appetitive conditioning (see also [40] or even the development of an aversion to the reward (after food-toxin pairings), the lesion eliminated the reward-devaluation effect. After an aversion to the reward was established, testing with the reward signal in sham animals yielded less responding after reward-toxin pairings than after unpaired reward and toxin presentations (the reward-devaluation effect); how- ever, animals with BLA lesions failed to display such response suppres- sion. Whereas this research points to a role of the BLA region in reward processes, there is less information on the amygdala's function in http://dx.doi.org/10.1016/j.bbr.2017.05.036 Received 10 April 2017; Received in revised form 8 May 2017; Accepted 10 May 2017 ⁎ Corresponding author. E-mail addresses: kkawasak@hoshi.ac.jp (K. Kawasaki), ivan.annicchiarico@gmail.com (I. Annicchiarico), glueckphd@gmail.com (A.C. Glueck), imoron@ugr.es (I. Morón), m.papini@tcu.edu (M.R. Papini). Behavioural Brain Research 331 (2017) 205–213 Available online 13 May 2017 0166-4328/ © 2017 Elsevier B.V. All rights reserved. MARK