Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour

Pavlovian conditioned cues exert a powerful influence on instrumental actions directed towards a common reward, this is known as Pavlovian‐to‐instrumental transfer (PIT). The nucleus accumbens (NAcc) has been hypothesized to function as an interface between limbic cortical structures required for associative conditioning, like the amygdala, and response mechanisms through which instrumental behaviour can be selected and performed. Here we have used selective excitotoxic lesions to investigate the involvement of subnuclei of the amygdala as well as the core and shell regions of the nucleus accumbens on PIT in rats. Within the amygdala, selective lesions of the central nucleus (CeN), but not of the basolateral nucleus (BLA), abolished the PIT effect. In addition, selective lesions of the NAcc core, but not the NAcc shell, also abolished PIT. None of the lesions impaired the acquisition of Pavlovian food cup approaches or instrumental responding itself. These data demonstrate that the CeN and NAcc core are central components of the neural system mediating the impact of Pavlovian cues on instrumental responding. We suggest that this effect may depend upon the regulation of the dopaminergic innervation of the NAcc core by projections from the CeN to the ventral tegmental area.

[1]  W. Estes Discriminative conditioning. I. A discriminative property of conditioned anticipation. , 1943 .

[2]  R. Rescorla,et al.  Two-process learning theory: Relationships between Pavlovian conditioning and instrumental learning. , 1967, Psychological review.

[3]  José M. R. Delgado,et al.  Integrative Activity of the Brain , 1968, The Yale Journal of Biology and Medicine.

[4]  E. Fonberg Amygdala functions within the alimentary system. , 1974, Acta neurobiologiae experimentalis.

[5]  E. Fonberg,et al.  Salivary reactions in dogs with dorsomedial amygdalar lesions. , 1975, Acta neurobiologiae experimentalis.

[6]  J. Price,et al.  Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat , 1978, The Journal of comparative neurology.

[7]  J. Pearce,et al.  The influence of context-reinforcer associations on instrumental performance , 1979 .

[8]  Douglas L. Jones,et al.  From motivation to action: Functional interface between the limbic system and the motor system , 1980, Progress in Neurobiology.

[9]  D. Amaral,et al.  An autoradiographic study of the projections of the central nucleus of the monkey amygdala , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  P. Lovibond Facilitation of instrumental behavior by a Pavlovian appetitive conditioned stimulus. , 1983, Journal of experimental psychology. Animal behavior processes.

[11]  L. Swanson The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[12]  H. Simon,et al.  Modulation of dopaminergic activity in the nucleus accumbens following facilitation or blockade of the dopaminergic transmission in the amygdala: a study by in vivo differential pulse voltammetry , 1985, Brain Research.

[13]  A. Dickinson,et al.  Pavlovian Processes in the Motivational Control of Instrumental Performance , 1987 .

[14]  J. Glowinski,et al.  Lesion of dopaminergic terminals in the amygdala produces enhanced locomotor response to d-amphetamine and opposite changes in dopaminergic activity in prefrontal cortex and nucleus accumbens , 1988, Brain Research.

[15]  T. Robbins,et al.  Involvement of the amygdala in stimulus-reward associations: Interaction with the ventral striatum , 1989, Neuroscience.

[16]  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.

[17]  Joseph E LeDoux,et al.  Topographic organization of neurons in the acoustic thalamus that project to the amygdala , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  M. Herkenham,et al.  Thalamoamygdaloid projections in the rat: A test of the amygdala's role in sensory processing , 1991, The Journal of comparative neurology.

[19]  T. Robbins,et al.  Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues , 1991, Neuroscience.

[20]  T. Robbins,et al.  The basolateral amygdala-ventral striatal system and conditioned place preference: Further evidence of limbic-striatal interactions underlying reward-related processes , 1991, Neuroscience.

[21]  D. S. Zahm,et al.  Specificity in the projection patterns of accumbal core and shell in the rat , 1991, Neuroscience.

[22]  T. Robbins,et al.  Functions of dopamine in the dorsal and ventral striatum , 1992 .

[23]  T. Robbins,et al.  Amygdala-ventral striatal interactions and reward-related processes. , 1992 .

[24]  L. Goldstein The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1992, The Yale Journal of Biology and Medicine.

[25]  D. S. Zahm,et al.  On the significance of subterritories in the “accumbens” part of the rat ventral striatum , 1992, Neuroscience.

[26]  Virendra B. Singh,et al.  Increase in cortical and midbrain tryptophan hydroxylase activity by intracerebroventricular administration of corticotropin releasing factor: block by adrenalectomy, by RU 38486 and by bilateral lesions to the central nucleus of the amygdala , 1992, Neurochemistry International.

[27]  Trevor W. Robbins,et al.  Differential effects of excitotoxic lesions of the basolateral amygdala, ventral subiculum and medial prefrontal cortex on responding with conditioned reinforcement and locomotor activity potentiated by intra-accumbens infusions ofd-amphetamine , 1993, Behavioural Brain Research.

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

[29]  B. Balleine,et al.  Effects of ibotenic acid lesions of the Nucleus Accumbens on instrumental action , 1994, Behavioural Brain Research.

[30]  B. Balleine Asymmetrical Interactions between Thirst and Hunger in Pavlovian-Instrumental Transfer , 1994, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[31]  R. Colwill,et al.  Encoding of the unconditioned stimulus in Pavlovian conditioning , 1994 .

[32]  A. Kelley,et al.  Glutamate receptors in the nucleus accumbens shell control feeding behavior via the lateral hypothalamus , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  S. B. Caine,et al.  Effects of the dopamine D-1 antagonist SCH 23390 microinjected into the accumbens, amygdala or striatum on cocaine self-administration in the rat , 1995, Brain Research.

[34]  T. Robbins,et al.  Effects of excitotoxic lesions of the central amygdaloid nucleus on the potentiation of reward-related stimuli by intra-accumbens amphetamine. , 1996, Behavioral neuroscience.

[35]  Effects of excitotoxic lesions of the central amygdaloid nucleus on the potentiation of reward-related stimuli by intra-accumbens amphetamine. , 1996, Behavioral neuroscience.

[36]  P. Holland,et al.  Neurotoxic Lesions of Basolateral, But Not Central, Amygdala Interfere with Pavlovian Second-Order Conditioning and Reinforcer Devaluation Effects , 1996, The Journal of Neuroscience.

[37]  H. Groenewegen,et al.  The nucleus accumbens: gateway for limbic structures to reach the motor system? , 1996, Progress in brain research.

[38]  S. Smith‐Roe,et al.  Response-reinforcement learning is dependent on N-methyl-D-aspartate receptor activation in the nucleus accumbens core. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Y. Hurd,et al.  In vivo Amygdala Dopamine Levels Modulate Cocaine Self‐administration Behaviour in the Rat: D1 Dopamine Receptor Involvement , 1997, The European journal of neuroscience.

[40]  Jonathan C. Gewirtz,et al.  Second-order fear conditioning prevented by blocking NMDA receptors in amygdala , 1997, Nature.

[41]  P. Holland,et al.  The Role of an Amygdalo-Nigrostriatal Pathway in Associative Learning , 1997, The Journal of Neuroscience.

[42]  V Bassareo,et al.  Differential Influence of Associative and Nonassociative Learning Mechanisms on the Responsiveness of Prefrontal and Accumbal Dopamine Transmission to Food Stimuli in Rats Fed Ad Libitum , 1997, The Journal of Neuroscience.

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

[44]  A. McDonald Cortical pathways to the mammalian amygdala , 1998, Progress in Neurobiology.

[45]  P. Holland,et al.  Amygdala circuitry in attentional and representational processes , 1999, Trends in Cognitive Sciences.

[46]  T. Robbins,et al.  Effects of excitotoxic lesions of the basolateral amygdala on conditional discrimination learning with primary and conditioned reinforcement , 1999, Behavioural Brain Research.

[47]  T. Robbins,et al.  Dissociation in Effects of Lesions of the Nucleus Accumbens Core and Shell on Appetitive Pavlovian Approach Behavior and the Potentiation of Conditioned Reinforcement and Locomotor Activity byd-Amphetamine , 1999, The Journal of Neuroscience.

[48]  J. Salamone,et al.  Nucleus accumbens dopamine and rate of responding: Neurochemical and behavioral studies , 1999, Psychobiology.

[49]  J. Mirenowicz,et al.  Dissociation of Pavlovian and instrumental incentive learning under dopamine antagonists. , 2000, Behavioral neuroscience.

[50]  S. Haber,et al.  The central nucleus of the amygdala projection to dopamine subpopulations in primates , 2000, Neuroscience.

[51]  B. Everitt,et al.  Limbic cortical-ventral striatal systems underlying appetitive conditioning. , 2000, Progress in brain research.

[52]  K. Berridge,et al.  Intra-Accumbens Amphetamine Increases the Conditioned Incentive Salience of Sucrose Reward: Enhancement of Reward “Wanting” without Enhanced “Liking” or Response Reinforcement , 2000, The Journal of Neuroscience.

[53]  Rudolf N. Cardinal,et al.  Differential involvement of amygdala subsystems in appetitive conditioning and drug addiction. , 2000 .

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

[55]  T. Robbins,et al.  Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: further evidence for limbic cortical-ventral striatopallidal systems. , 2000, Behavioral neuroscience.

[56]  Joseph E LeDoux,et al.  Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus , 2000, Nature Neuroscience.

[57]  Robert L. Mason,et al.  Statistical Principles in Experimental Design , 2003 .