The amygdala and reward

Baxter, Mark G.; Murray, Elisabeth A.

doi:10.1038/nrn875

Cited by 1,200Memory and Neural MechanismsNeural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on Behavior

The amygdala and reward

Baxter, Mark G., Murray, Elisabeth A.·2002·Nature Reviews Neuroscience

DOI 10.1038/nrn875

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Abstract

The amygdala -- an almond-shaped group of nuclei at the heart of the telencephalon -- has been associated with a range of cognitive functions, including emotion, learning, memory, attention and perception. Most current views of amygdala function emphasize its role in negative emotions, such as fear, and in linking negative emotions with other aspects of cognition, such as learning and memory. However, recent evidence supports a role for the amygdala in processing positive emotions as well as negative ones, including learning about the beneficial biological value of stimuli. Indeed, the amygdala's role in stimulus-reward learning might be just as important as its role in processing negative affect and fear conditioning.

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Amygdala and striatum have well-documented anatomic connectivity and show tight functional coupling in stimulus-reward association and stimulus-cue devaluation.
“Amygdala and striatum have a well-documented anatomic connectivity (29) and show a tight functional coupling in stimulus–reward association and stimulus–cue devaluation (30).”
From Amygdala damage eliminates monetary loss aversion (2010) · cites this paper as [30]
Both the amygdala and hippocampus are known to mediate attentional and learning aspects of emotion.
“Both the amygdala and hippocampus are known to mediate attentional and learning aspects of emotion (Baxter and Murray, 2002, Calder et al., 2001; Phelps, 2004; Phelps and LeDoux, 2005).”
From Adolescent neurobiological susceptibility to social context (2016) · cites this paper as Baxter and Murray, 2002

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Amygdala and the memory of reward: the importance of fibres of passage from the basal forebrain
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Reinforcer devaluation abolishes conditioned cue preference: Evidence for stimulus-stimulus associations.
Yin, H. H., & Knowlton, B. J. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.1.174 · Cited by 27 · see citing works
Reinterpreting the behavioural effects of amygdala lesions in non-human primates
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Reinforcer devaluation abolishes conditioned cue preference: Evidence for stimulus-stimulus associations.
Yin, H. H., & Knowlton, B. J. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.1.174 · Cited by 15 · see citing works

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The reward circuit: linking primate anatomy and human imaging
Haber, S. N., & Knutson, B. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.129 · Cited by 3,718 · see citing works
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Untitled work
(2009)
Are Emotions Natural Kinds?
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“Once the association is formed, the CS itself has the ability to elicit innate defense responses.”
Frames, Biases, and Rational Decision-Making in the Human Brain
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The neurobiology of anhedonia and other reward-related deficits
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The human amygdala and the emotional evaluation of sensory stimuli
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a neurobehavioral model of affiliative bonding: implications for conceptualizing a human trait of affiliation
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Distant influences of amygdala lesion on visual cortical activation during emotional face processing
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The primate amygdala represents the positive and negative value of visual stimuli during learning
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What does the amygdala contribute to social cognition
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The hidden island of addiction: the insula
Naqvi, N. H., & Bechara, A. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2008.09.009 · Cited by 833 · see citing works
Processing of primary and secondary rewards: A quantitative meta-analysis and review of human functional neuroimaging studies
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The dual pathway model of AD/HD: an elaboration of neuro-developmental characteristics
Sonuga-Barke, E. J. S. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2003.08.005 · Cited by 816 · see citing works
Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation
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Predictors of amygdala activation during the processing of emotional stimuli: A meta-analysis of 385 PET and fMRI studies
Costafreda, S. G., Brammer, M. J., David, A. S., & Fu, C. H. Y. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.10.012 · Cited by 772 · see citing works
Reward mechanisms in obesity: new insights and future directions
Kenny, P. J. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.016 · Cited by 748 · see citing works
Triadic model of the neurobiology of motivated behavior in adolescence.
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A systems approach to appraisal mechanisms in emotion
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Brain mechanisms for emotional influences on perception and attention: What is magic and what is not
Pourtois, G., Schettino, A., & Vuilleumier, P. (2013) · Biological Psychology · doi:10.1016/j.biopsycho.2012.02.007 · Cited by 687 · see citing works
Ghrelin Modulates Brain Activity in Areas that Control Appetitive Behavior
Malik, S., McGlone, F., Bedrossian, D., & Dagher, A. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2008.03.007 · Cited by 677 · see citing works
The amygdala, reward and emotion
Murray, E. A. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.08.013 · Cited by 679 · see citing works
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The Role of Neural Plasticity in Depression: From Hippocampus to Prefrontal Cortex
Liu, W., Ge, T., Leng, Y., Pan, Z., Fan, J., Yang, W., & Cui, R. (2017) · Neural Plasticity · doi:10.1155/2017/6871089 · Cited by 640 · see citing works
A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing
Tottenham, N. (2009) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.068.2009 · Cited by 651 · see citing works
Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents.
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Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task
Wallis, J. D., & Miller, E. K. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02922.x · Cited by 628 · see citing works
The first taste is always with the eyes: A meta-analysis on the neural correlates of processing visual food cues
van der Laan, L. N., de Ridder, D. T. D., Viergever, M. A., & Smeets, P. A. M. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.11.055 · Cited by 602 · see citing works
Emotion, Cognition, and Mental State Representation in Amygdala and Prefrontal Cortex
Salzman, C., & Fusi, S. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135256 · Cited by 581 · see citing works
Anatomy of a decision: Striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal.
Frank, M. J., & Claus, E. D. (2006) · Psychological Review · doi:10.1037/0033-295x.113.2.300 · Cited by 578 · see citing works
Cortical and limbic activation during viewing of high- versus low-calorie foods
Killgore, W. D. S., Young, A. D., Femia, L. A., Bogorodzki, P., Rogowska, J., & Yurgelun-Todd, D. A. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00191-5 · Cited by 581 · see citing works
Neurobiology of Decision Making: A Selective Review from a Neurocognitive and Clinical Perspective
Monique Ernst, D., & Paulus, M. P. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.06.004 · Cited by 567 · see citing works
Hyperdopaminergic mutant mice have higher "wanting" but not "liking" for sweet rewards
Peciña, S., Cagniard, B., Berridge, K. C., Aldridge, J. W., & Zhuang, X. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-28-09395.2003 · Cited by 551 · see citing works
Absolute Coding of Stimulus Novelty in the Human Substantia Nigra/VTA
Bunzeck, N., & Düzel, E. (2006) · Neuron · doi:10.1016/j.neuron.2006.06.021 · Cited by 503 · see citing works
Neural Representation of Subjective Value Under Risk and Ambiguity
Levy, I., Snell, J., Nelson, A. J., Rustichini, A., & Glimcher, P. W. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00853.2009 · Cited by 491 · see citing works
A review of fronto-striatal and fronto-cortical brain abnormalities in children and adults with Attention Deficit Hyperactivity Disorder (ADHD) and new evidence for dysfunction in adults with ADHD during motivation and attention
Cubillo, A., Halari, R., Smith, A., Taylor, E., & Rubia, K. (2012) · Cortex · doi:10.1016/j.cortex.2011.04.007 · Cited by 505 · see citing works
Orbitofrontal cortex, decision-making and drug addiction
Schoenbaum, G., Roesch, M. R., & Stalnaker, T. A. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2005.12.006 · Cited by 499 · see citing works
The neural substrates of reward processing in humans: the modern role of FMRI
McClure, S. M., York, M. K., & Montague, P. R. (2004) · The Neuroscientist · doi:10.1177/1073858404263526 · Cited by 480 · see citing works
The development of psychopathy
Blair, J., Peschardt, K. S., Budhani, S., Mitchell, D. G. V., & Pine, D. S. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01596.x · Cited by 486 · see citing works
High-resolution magnetic resonance imaging reveals nuclei of the human amygdala: manual segmentation to automatic atlas
Saygin, Z. M., Kliemann, D., Iglesias, J. E., van der Kouwe, A. J. W., Boyd, E. C., Reuter, M., Stevens, A. A., Leemput, K. V., McKee, A. C., Frosch, M. P., et al. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.04.046 · Cited by 456 · see citing works
Effects of mindful-attention and compassion meditation training on amygdala response to emotional stimuli in an ordinary, non-meditative state
Desbordes, G., Negi, L. T., Pace, T. W. W., Wallace, B. A., Raison, C. L., & Schwartz, E. L. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00292 · Cited by 458 · see citing works
Food and drug cues activate similar brain regions: A meta-analysis of functional MRI studies
Tang, D., Fellows, L. K., Small, D. M., & Dagher, A. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.03.009 · Cited by 457 · see citing works
Amygdala damage eliminates monetary loss aversion
De Martino, B., Camerer, C. F., & Adolphs, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910230107 · Cited by 444 · see citing works
“Cool” Inferior Frontostriatal Dysfunction in Attention-Deficit/Hyperactivity Disorder Versus “Hot” Ventromedial Orbitofrontal-Limbic Dysfunction in Conduct Disorder: A Review
Rubia, K. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.09.023 · Cited by 440 · see citing works
Humor Modulates the Mesolimbic Reward Centers
Mobbs, D., Greicius, M. D., Abdel-Azim, E., Menon, V., & Reiss, A. L. (2003) · Neuron · doi:10.1016/s0896-6273(03)00751-7 · Cited by 440 · see citing works
The brain response to personally familiar faces in autism: Findings of fusiform activity and beyond
Pierce, K. (2004) · Brain · doi:10.1093/brain/awh289 · Cited by 432 · see citing works
An investigation of the structural, connectional, and functional subspecialization in the human amygdala
Bzdok, D., Laird, A. R., Zilles, K., Fox, P. T., & Eickhoff, S. B. (2012) · Human Brain Mapping · doi:10.1002/hbm.22138 · Cited by 430 · see citing works
GLP-1 Receptor Activation Modulates Appetite- and Reward-Related Brain Areas in Humans
van Bloemendaal, L., IJzerman, R. G., ten Kulve, J. S., Barkhof, F., Konrad, R. J., Drent, M. L., Veltman, D. J., & Diamant, M. (2014) · Diabetes · doi:10.2337/db14-0849 · Cited by 427 · see citing works
Overlapping Brain Circuits for Homeostatic and Hedonic Feeding
Rossi, M. A., & Stuber, G. D. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2017.09.021 · Cited by 415 · see citing works
Prospect theory on the brain? Toward a cognitive neuroscience of decision under risk
Trepel, C., Fox, C. R., & Poldrack, R. A. (2005) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2005.01.016 · Cited by 400 · see citing works
Valence is a basic building block of emotional life
Barrett, L. F. (2005) · Journal of Research in Personality · doi:10.1016/j.jrp.2005.08.006 · Cited by 402 · see citing works
Motivational systems in adolescence: Possible implications for age differences in substance abuse and other risk-taking behaviors
Doremus-Fitzwater, T. L., Varlinskaya, E. I., & Spear, L. P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.08.008 · Cited by 397 · see citing works
Common and distinct neural responses during direct and incidental processing of multiple facial emotions
Winston, J. S., O’Doherty, J. P., & Dolan, R. J. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00303-3 · Cited by 398 · see citing works
Neural Correlates of Processing Valence and Arousal in Affective Words
Lewis, P., Critchley, H., Rotshtein, P., & Dolan, R. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhk024 · Cited by 391 · see citing works
Contextual modulation of amygdala responsivity to surprised faces
Kim, H., Somerville, L. H., Johnstone, T., Polis, S., Alexander, A. L., Shin, L. M., & Whalen, P. J. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/0898929042947865 · Cited by 389 · see citing works
Basal ganglia orient eyes to reward
Hikosaka, O., Nakamura, K., & Nakahara, H. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00458.2005 · Cited by 377 · see citing works
Amygdala–frontal interactions and reward expectancy
Holland, P. C., & Gallagher, M. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.007 · Cited by 390 · see citing works
Applying a cognitive neuroscience perspective to the disorder of psychopathy
Blair, R. J. (2005) · Development and Psychopathology · doi:10.1017/s0954579405050418 · Cited by 418 · see citing works
Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants
Nitschke, J. B., Nelson, E. E., Rusch, B. D., Fox, A. S., Oakes, T. R., & Davidson, R. J. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.10.005 · Cited by 371 · see citing works
Oxytocin, motivation and the role of dopamine
Love, T. M. (2014) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.06.011 · Cited by 369 · see citing works
Effort discounting in human nucleus accumbens
Botvinick, M., Huffstetler, S., & McGuire, J. T. (2009) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.9.1.16 · Cited by 364 · see citing works
Abnormal ventromedial prefrontal cortex function in children with psychopathic traits during reversal learning
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Brain systems for assessing facial attractiveness
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“Liking” and “wanting” in eating and food reward: Brain mechanisms and clinical implications
Morales, I., & Berridge, K. C. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113152 · Cited by 346 · see citing works
Differential roles of human striatum and amygdala in associative learning
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Hippocampus and Amygdala Morphology in Attention-Deficit/Hyperactivity Disorder
Plessen, K. J., Bansal, R., Zhu, H., Whiteman, R., Amat, J., Quackenbush, G. A., Martin, L., Durkin, K., Blair, C., Royal, J., et al. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.7.795 · Cited by 347 · see citing works
Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala
Belova, M. A., Paton, J. J., Morrison, S. E., & Salzman, C. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.08.004 · Cited by 349 · see citing works
Meta-Analysis of Functional Neuroimaging Studies of Emotion Perception and Experience in Schizophrenia
Taylor, S. F., Kang, J., Brege, I. S., Tso, I. F., Hosanagar, A., & Johnson, T. D. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.09.007 · Cited by 341 · see citing works
On the Consumption of Negative Feelings
Andrade, E. B., & Cohen, J. B. (2007) · Journal of Consumer Research · doi:10.1086/519498 · Cited by 340 · see citing works
Pathophysiology of obsessive–compulsive disorder
Aouizerate, B., Guehl, D., Cuny, E., Rougier, A., Bioulac, B., Tignol, J., & Burbaud, P. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.02.004 · Cited by 341 · see citing works
Re-valuing the amygdala
Morrison, S. E., & Salzman, C. D. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.02.007 · Cited by 341 · see citing works
Emotion, decision making, and the amygdala.
Seymour, B., & Dolan, R. (2008) · Neuron · doi:10.1016/j.neuron.2008.05.020 · Cited by 324 · see citing works
Neural systems of positive affect: relevance to understanding child and adolescent depression?
FORBES, E. E., & DAHL, R. E. (2005) · Development and Psychopathology · doi:10.1017/s095457940505039x · Cited by 318 · see citing works
Trait and state anxiety are mapped differently in the human brain
Saviola, F., Pappaianni, E., Monti, A., Grecucci, A., Jovicich, J., & Pisapia, N. D. (2020) · Scientific Reports · doi:10.1038/s41598-020-68008-z · Cited by 319 · see citing works
The neural basis of drug stimulus processing and craving: an activation likelihood estimation meta-analysis
Chase, H. W., Eickhoff, S. B., Laird, A. R., & Hogarth, L. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.025 · Cited by 316 · see citing works
Homeostatic circuits selectively gate food cue responses in insular cortex
Livneh, Y., Ramesh, R. N., Burgess, C. R., Levandowski, K. M., Madara, J. C., Fenselau, H., Goldey, G. J., Diaz, V. E., Jikomes, N., Resch, J. M., et al. (2017) · Nature · doi:10.1038/nature22375 · Cited by 316 · see citing works
Viewing Pictures of a Romantic Partner Reduces Experimental Pain: Involvement of Neural Reward Systems
Younger, J., Aron, A., Parke, S., Chatterjee, N., & Mackey, S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013309 · Cited by 314 · see citing works
Motivational Salience: Amygdala Tuning From Traits, Needs, Values, and Goals
Cunningham, W. A., & Brosch, T. (2012) · Current Directions in Psychological Science · doi:10.1177/0963721411430832 · Cited by 312 · see citing works
Organization of valence-encoding and projection-defined neurons in the basolateral amygdala
Beyeler, A., Chang, C.-J., Silvestre, M., Lévêque, C., Namburi, P., Wildes, C. P., & Tye, K. M. (2018) · Cell Reports · doi:10.1016/j.celrep.2017.12.097 · Cited by 306 · see citing works
“…inputs and is necessary for the acquisition of fear conditioning (Fanselow and Kim, 1994; LeDoux et al., 1990; Maren and Quirk, 2004; Miserendino et al., 1990; Wilensky et al., 1999) and reward associations (Baxter and Murray, 2002; Cador et al., 1989; Cardinal et al., 2002; Tye et al., 2008).”
Background
The basolateral amygdala in reward learning and addiction
Wassum, K. M., & Izquierdo, A. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.08.017 · Cited by 306 · see citing works
Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings
Dichter, G. S., Damiano, C. A., & Allen, J. A. (2012) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-4-19 · Cited by 299 · see citing works
The neuroscience of positive emotions and affect: Implications for cultivating happiness and wellbeing
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Immediate Reward Bias in Humans: Fronto-Parietal Networks and a Role for the Catechol-<i>O</i>-Methyltransferase 158<sup>Val/Val</sup>Genotype
Boettiger, C. A., Mitchell, J. M., Tavares, V. C., Robertson, M., Joslyn, G., D'Esposito, M., & Fields, H. L. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2551-07.2007 · Cited by 300 · see citing works
Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data
Spear, L. P. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.08.001 · Cited by 292 · see citing works
Putting Reward in Art: A Tentative Prediction Error Account of Visual Art
de Cruys, S. V., & Wagemans, J. P. (2011) · i-Perception · doi:10.1068/i0466aap · Cited by 296 · see citing works
Lesions of medial prefrontal cortex disrupt the acquisition but not the expression of goal-directed learning.
Ostlund, S. B., & Balleine, B. W. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1921-05.2005 · Cited by 291 · see citing works
Mood, food, and obesity
Singh, M. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.00925 · Cited by 337 · see citing works
Localization of Deformations Within the Amygdala in Individuals With Psychopathy
Yang, Y., Raine, A., Narr, K. L., Colletti, P. M., & Toga, A. W. (2009) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2009.110 · Cited by 284 · see citing works
Individual differences in extraversion and dopamine genetics predict neural reward responses
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Neuronal connectivity and interactions between the auditory and limbic systems. Effects of noise and tinnitus
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Authors: Baxter, M. G., & Murray, E. A.
Affiliations: Harvard University (US)
National Institutes of Health (US)
ORCID: Baxter, Mark G.
Murray, Elisabeth A.
Venue: Nature Reviews Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2002-07-01
Volume: 3
Issue: 7
Pages: 563-573
ISSN: 1471-003X (ISSN-L)
1471-0048
DOI: 10.1038/nrn875
OpenAlex: W2085971650
Cited by: 1,200
References: 91
Citations by year: 2026: 20 · 2025: 27 · 2024: 39 · 2023: 31 · 2022: 46 · 2021: 44 · 2020: 80 · 2019: 48 · 2018: 45 · 2017: 45 · 2016: 40 · 2015: 59 · 2014: 75 · 2013: 59 · 2012: 58
FWCI: 3.97
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature reviews. Neuroscience (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: amygdala, reward, positive emotions, fear conditioning, emotional learning, memory, emotion and cognition
MeSH terms: Amygdala, Animals, Haplorhini, Association, Behavior, Animal, Choice Behavior, Discrimination Learning, Photic Stimulation, Reward, Smell, Prefrontal Cortex, Rats

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