Differential involvement of the central amygdala in appetitive versus aversive learning.

Understanding the function of the distinct amygdaloid nuclei in learning comprises a major challenge. In the two studies described herein, we used c-Fos immunolabeling to compare the engagement of various nuclei of the amygdala in appetitive and aversive instrumental training procedures. In the first experiment, rats that had already acquired a bar-pressing response to a partial food reinforcement were further trained to learn that an acoustic stimulus signaled either continuous food reinforcement (appetitive training) or a footshock (aversive training). The first training session of the presentation of the acoustic stimulus resulted in significant increases of c-Fos immunolabeling throughout the amygdala; however, the pattern of activation of the nuclei of the amygdala differed according to the valence of motivation. The medial part of the central amygdala (CE) responded, surprisingly, to the appetitive conditioning selectively. The second experiment was designed to extend the aversive versus appetitive conditioning to mice, trained either for place preference or place avoidance in an automated learning system (INTELLICAGE). Again, much more intense c-Fos expression was observed in the medial part of the CE after the appetitive training as compared to the aversive training. These data, obtained in two species and by means of novel experimental approaches balancing appetitive versus aversive conditioning, support the hypothesis that the central nucleus of the amygdala is particularly involved in appetitively motivated learning processes.

[1]  A. Dickinson,et al.  Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour , 2001, The European journal of neuroscience.

[2]  B. Balleine,et al.  Motivational control of goal-directed action , 1994 .

[3]  L. Kaczmarek Molecular biology of vertebrate learning: Is c‐fos a new beginning? , 1993, Journal of neuroscience research.

[4]  M. Gallagher,et al.  Amygdala central nucleus lesions disrupt increments, but not decrements, in conditioned stimulus processing. , 1993, Behavioral neuroscience.

[5]  C. Dayas,et al.  Neuroendocrine responses to an emotional stressor: evidence for involvement of the medial but not the central amygdala , 1999, The European journal of neuroscience.

[6]  F. Graeff,et al.  Differential expression of Fos protein in the rat brain induced by performance of avoidance or escape in the elevated T-maze , 2001, Behavioural Brain Research.

[7]  C. Le Moine,et al.  A Specific Limbic Circuit Underlies Opiate Withdrawal Memories , 2005, The Journal of Neuroscience.

[8]  P. Holland,et al.  Role of Amygdalo-Nigral Circuitry in Conditioning of a Visual Stimulus Paired with Food , 2005, The Journal of Neuroscience.

[9]  M. Fanselow,et al.  The Amygdala and Fear Conditioning: Has the Nut Been Cracked? , 1996, Neuron.

[10]  T. Robbins,et al.  Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala , 1997, Nature.

[11]  A. Vyssotski,et al.  A comparison of wild-caught wood mice and bank voles in the Intellicage: assessing exploration, daily activity patterns and place learning paradigms , 2005, Behavioural Brain Research.

[12]  M. Gallagher,et al.  The amygdala complex: multiple roles in associative learning and attention. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[13]  M. Gallagher,et al.  The amygdala central nucleus and appetitive Pavlovian conditioning: lesions impair one class of conditioned behavior , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  T. Humphrey The telencephalon of the bat. I. The non‐cortical nuclear masses and certain pertinent fiber connections , 1936 .

[15]  James L Olds,et al.  AMYGDALOID STIMULATION AND OPERANT REINFORCEMENT IN THE RAT. , 1963, Journal of comparative and physiological psychology.

[16]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[17]  T. Otto,et al.  Patterns of Fos expression in the amygdala and ventral perirhinal cortex induced by training in an olfactory fear conditioning paradigm. , 2001, Behavioral neuroscience.

[18]  Ja Wook Koo,et al.  Behavioral / Systems / Cognitive Selective Neurotoxic Lesions of Basolateral and Central Nuclei of the Amygdala Produce Differential Effects on Fear Conditioning , 2004 .

[19]  Humphrey Tryphena TELENCEPHALON OF THE BAT , 1937 .

[20]  E. Jolkkonen,et al.  Anatomic heterogeneity of the rat amygdaloid complex. , 2000, Folia morphologica.

[21]  M. Petrides,et al.  Ibotenic acid lesions of the basolateral, but not the central, amygdala interfere with conditioned taste aversion: evidence from a combined behavioral and anatomical tract-tracing investigation. , 1999, Behavioral neuroscience.

[22]  L. Kaczmarek,et al.  Defensive conditioning-related functional heterogeneity among nuclei of the rat amygdala revealed by c-Fos mapping , 1999, Neuroscience.

[23]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[24]  K. Taghzouti,et al.  Increase of the aversive value of taste stimuli following ibotenic acid lesion of the central amygdaloid nucleus in the rat , 1997, Behavioural Brain Research.

[25]  J. Power,et al.  The amygdaloid complex: anatomy and physiology. , 2003, Physiological reviews.

[26]  G. Lynch,et al.  Differential patterns of c-fos mRNA expression in amygdala during successive stages of odor discrimination learning. , 1997, Learning & memory.

[27]  M. Fanselow,et al.  Immediate-early gene expression in the amygdala following footshock stress and contextual fear conditioning , 1998, Brain Research.

[28]  T. Robbins,et al.  Effects of selective excitotoxic lesions of the nucleus accumbens core, anterior cingulate cortex, and central nucleus of the amygdala on autoshaping performance in rats. , 2002, Behavioral neuroscience.

[29]  L. Kaczmarek Chapter VIII c-Fos in learning: beyond the mapping of neuronal activity , 2002 .

[30]  A. Kelley Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning , 2004, Neuroscience & Biobehavioral Reviews.

[31]  T. Robbins,et al.  Dissociable roles of the central and basolateral amygdala in appetitive emotional learning , 2000, The European journal of neuroscience.

[32]  Theresa M. Desrochers,et al.  Two different lateral amygdala cell populations contribute to the initiation and storage of memory , 2001, Nature Neuroscience.

[33]  L. Kaczmarek,et al.  Differential response of two subdivisions of lateral amygdala to aversive conditioning as revealed by c-Fos and P-ERK mapping , 2002, Neuroreport.

[34]  Charles F Stevens,et al.  Synaptic plasticity , 1998, Current Biology.

[35]  G. Coover,et al.  Effects of small amygdala lesions on fear, but not aggression, in the rat , 1997, Physiology & Behavior.

[36]  Trevor W Robbins,et al.  Appetitive Behavior , 2003, Annals of the New York Academy of Sciences.

[37]  L. Kaczmarek,et al.  C-fos protooncogene expression in rat brain after long-term training of two-way active avoidance reaction , 1992, Behavioural Brain Research.

[38]  George R. Breese,et al.  Neuroanatomical characterization of Fos induction in rat behavioral models of anxiety , 1996, Brain Research.

[39]  J. Johnston Further contributions to the study of the evolution of the forebrain , 1923 .

[40]  A. Chiba,et al.  The amygdala and emotion , 1996, Current Opinion in Neurobiology.

[41]  Joseph E LeDoux,et al.  Emotion: Systems, Cells, Synaptic Plasticity , 1996, Cell.

[42]  J. Radulovic,et al.  Relationship between Fos Production and Classical Fear Conditioning: Effects of Novelty, Latent Inhibition, and Unconditioned Stimulus Preexposure , 1998, The Journal of Neuroscience.

[43]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[44]  P. Holland,et al.  Double dissociation of the effects of lesions of basolateral and central amygdala on conditioned stimulus‐potentiated feeding and Pavlovian‐instrumental transfer , 2003, The European journal of neuroscience.

[45]  E. Murray,et al.  The amygdala and reward , 2002, Nature Reviews Neuroscience.

[46]  M. Holahan,et al.  Conditioned Memory Modulation, Freezing, and Avoidance as Measures of Amygdala-Mediated Conditioned Fear , 2002, Neurobiology of Learning and Memory.

[47]  O. Stiedl,et al.  Production of the Fos protein after contextual fear conditioning of C57BL/6N mice , 1998, Brain Research.