Contributions of the Amygdala to Reward Expectancy and Choice Signals in Human Prefrontal Cortex
Open accessAbstract
The prefrontal cortex (PFC) receives substantial anatomical input from the amygdala, and these two structures have long been implicated in reward-related learning and decision making. Yet little is known about how these regions interact, especially in humans. We investigated the contribution of the amygdala to reward-related signals in PFC by scanning two rare subjects with focal bilateral amygdala lesions using fMRI. The subjects performed a reversal learning task in which they first had to learn which of two choices was the more rewarding, and then flexibly switch their choices when contingencies changed. Compared with healthy controls, both amygdala lesion subjects showed a profound change in ventromedial prefrontal cortex (vmPFC) activity associated with reward expectation and behavioral choice. These findings support a critical role for the human amygdala in establishing expected reward representations in PFC, which in turn may be used to guide behavioral choice.
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The amygdala's role in mediating loss aversion may be analogous to its role in modulating caudate- or hippocampal-dependent memory and choice in reversal tasks.
“In this regard, the amygdala’s role in mediating loss aversion may be analogous to its role in modulating caudate- or hippocampal-dependent memory (31), and choice in reversal tasks (20).”
From Amygdala damage eliminates monetary loss aversion (2010) · cites this paper as [20]
Cites
Insensitivity to future consequences following damage to human prefrontal cortex
Bechara, A., Damasio, A. R., Damasio, H., & Anderson, S. W. (1994) · Cognition · doi:10.1016/0010-0277(94)90018-3 · Cited by 6,128 · see citing works
Spatial registration and normalization of images
Friston, K. J., Ashburner, J., Frith, C., Poline, J.-B., Heather, J. D., & Frackowiak, R. S. J. (1995) · Human Brain Mapping · doi:10.1002/hbm.460030303 · Cited by 3,744 · see citing works
Mathematical Statistics and Data Analysis
Rabinowitz, L., & Rice, J. A. (1989) · Technometrics · doi:10.2307/3556160 · Cited by 3,142 · see citing works
Cortical substrates for exploratory decisions in humans
Daw, N. D., O'Doherty, J. P., Dayan, P., Seymour, B., & Dolan, R. J. (2006) · Nature · doi:10.1038/nature04766 · Cited by 2,224 · see citing works
Self-citationAbstract reward and punishment representations in the human orbitofrontal cortex
O'Doherty, J., Kringelbach, M. L., Rolls, E. T., Hornak, J., & Andrews, C. (2001) · Nature Neuroscience · doi:10.1038/82959 · Cited by 2,003 · see citing works
Self-citationBechara, A., Tranel, D., & Damásio, H. (2000) · Brain · doi:10.1093/brain/123.11.2189 · Cited by 1,919 · see citing works
The Orbitofrontal Cortex and Reward
Rolls, E. T. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.284 · Cited by 1,595 · see citing works
Relative reward preference in primate orbitofrontal cortex
Tremblay, L., & Schultz, W. (1999) · Nature · doi:10.1038/19525 · Cited by 1,314 · see citing works
Dissociation of reward anticipation and outcome with event-related fMRI
Knutson, B., Fong, G. W., Adams, C. M., Varner, J. L., & Hommer, D. (2001) · Neuroreport · doi:10.1097/00001756-200112040-00016 · Cited by 1,300 · see citing works
Baxter, M. G., & Murray, E. A. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn875 · Cited by 1,200 · see citing works
Changes in brain activity related to eating chocolate: From pleasure to aversion
Small, D. M. (2001) · Brain · doi:10.1093/brain/124.9.1720 · Cited by 1,179 · cited 3× · see citing works
“When comparing responses to receipt of rewarding outcomes compared with punishing ones, in our control subjects we found significant activity relating to receipt of reward in medial PFC and medial OFC (Figure 6A), consistent with previous reports (Anderson et al., 2003; Knutson et al., 2001; O’Doherty et al., 2001, 20…”
Amygdalo‐cortical projections in the monkey ( <i>Macaca fascicularis</i> )
Amaral, D. G., & Price, J. L. (1984) · Journal of Comparative Neurology · doi:10.1002/cne.902300402 · Cited by 1,162 · see citing works
Dorsal anterior cingulate cortex: A role in reward-based decision making
Bush, G., Vogt, B. A., Holmes, J., Dale, A. M., Greve, D., Jenike, M. A., & Rosen, B. R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.012470999 · Cited by 1,096 · see citing works
Dissociated neural representations of intensity and valence in human olfaction
Anderson, A. K., Christoff, K., Stappen, I., Panitz, D., Ghahremani, D. G., Glover, G., Gabrieli, J. D. E., & Sobel, N. (2003) · Nature Neuroscience · doi:10.1038/nn1001 · Cited by 1,054 · see citing works
Rolls, E. T., Hornak, J., Wade, D., & McGrath, J. (1994) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.57.12.1518 · Cited by 1,005 · see citing works
The Anatomical Connections of the Macaque Monkey Orbitofrontal Cortex. A Review
Cavada, C. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.220 · Cited by 917 · see citing works
The primate amygdala represents the positive and negative value of visual stimuli during learning
Paton, J. J., Belova, M. A., Morrison, S. E., & Salzman, C. D. (2006) · Nature · doi:10.1038/nature04490 · Cited by 917 · cited 1× · see citing works
“Single-unit studies have found that neurons in both structures respond to stimulus cues predictive of future rewarding or punishing outcomes, or respond in anticipation of an impending outcome (Paton et al., 2006; Schoenbaum et al., 1998, 2003; Thorpe et al., 1983; Tremblay and Schultz, 1999).”
BackgroundBeauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness
O’Doherty, J., Winston, J., Critchley, H., Perrett, D., Burt, D. M., & Dolan, R. J. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(02)00145-8 · Cited by 898 · see citing works
Self-citationOrbitofrontal cortex and basolateral amygdala encode expected outcomes during learning
Schoenbaum, G. M., Chiba, A. A., & Gallagher, M. (1998) · Nature Neuroscience · doi:10.1038/407 · Cited by 849 · see citing works
The orbitofrontal cortex: Neuronal activity in the behaving monkey
Thorpe, S. J., Rolls, E. T., & Maddison, S. (1983) · Experimental Brain Research · doi:10.1007/bf00235545 · Cited by 836 · see citing works
Cools, R., Clark, L., Owen, A. M., & Robbins, T. W. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-11-04563.2002 · Cited by 784 · see citing works
Iversen, S., & Mishkin, M. (1970) · Experimental Brain Research · doi:10.1007/bf00237911 · Cited by 765 · see citing works
Amygdala-prefrontal coupling depends on a genetic variation of the serotonin transporter
Heinz, A., Braus, D. F., Smolka, M. N., Wrase, J., Puls, I., Hermann, D., Vollstädt‐Klein, S., Grüsser, S. M., Flor, H., Schumann, G., et al. (2004) · Nature Neuroscience · doi:10.1038/nn1366 · Cited by 700 · see citing works
Regret and its avoidance: a neuroimaging study of choice behavior
Coricelli, G., Critchley, H., Joffily, M., O’Doherty, J. P., Angela Sirigu, B., & Dolan, R. J. (2005) · Nature Neuroscience · doi:10.1038/nn1514 · Cited by 673 · see citing works
Self-citationO'Doherty, J., Critchley, H., Deichmann, R., & Dolan, R. J. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-21-07931.2003 · Cited by 611 · see citing works
Self-citationBaxter, M. G., Parker, A., Lindner, C. C. C., Izquierdo, A. D., & Murray, E. A. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04311.2000 · Cited by 582 · see citing works
Hatfield, T., Han, J.-S., Conley, M., Gallagher, M., & Holland, P. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-16-05256.1996 · Cited by 555 · see citing works
Hampton, A. N., Bossaerts, P., & O’Doherty, J. P. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1010-06.2006 · Cited by 498 · see citing works
Self-citationSchoenbaum, G., Setlow, B., Saddoris, M. P., & Gallagher, M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00474-4 · Cited by 484 · 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
IMAGING VALUATION MODELS IN HUMAN CHOICE
Montague, P. R., King‐Casas, B., & Cohen, J. D. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112903 · Cited by 371 · see citing works
Málková, L., Gaffan, D., & Murray, E. A. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-15-06011.1997 · Cited by 295 · see citing works
Kilpatrick, L. A. (2003) · NeuroImage · doi:10.1016/j.neuroimage.2003.08.006 · Cited by 294 · see citing works
Gottfried, J. A., Smith, A. P. R., Rugg, M. D., & Dolan, R. J. (2004) · Neuron · doi:10.1016/s0896-6273(04)00270-3 · Cited by 261 · see citing works
Iidaka, T., Omori, M., Murata, T., Kosaka, H., Yonekura, Y., Okada, T., & Sadato, N. (2001) · Journal of Cognitive Neuroscience · doi:10.1162/089892901753294338 · Cited by 233 · see citing works
Basolateral Amygdala Lesions Abolish Orbitofrontal-Dependent Reversal Impairments
Stalnaker, T. A., Franz, T. M., Singh, T., & Schoenbaum, G. M. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.014 · Cited by 178 · see citing works
Izquierdo, A., & Murray, E. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00968.2003 · Cited by 172 · see citing works
Selective bilateral amygdala lesions in rhesus monkeys fail to disrupt object reversal learning
Izquierdo, A., & Murray, E. A. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3616-06.2007 · Cited by 121 · see citing works
Hofer, P. (1973) · PubMed · Cited by 79 · see citing works
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The theory of constructed emotion: an active inference account of interoception and categorization
Barrett, L. F. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw154 · Cited by 1,426 · see citing works
“…amygdala lesions (Bechara et al., 1995, 1999; Adolphs et al., 1999; Adolphs and Tranel, 1999, 2003; Atkinson et al., 2007; de Gelder et al., 2014; Hampton et al., 2007; Tsuchiya et al., 2009; Hurlemann et al., 2007; De Martino et al., 2010; Boes et al., 2011; Feinstein et al., 2011, 2013, 2016;…”
Hiser, J., & Koenigs, M. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.030 · Cited by 972 · see citing works
The theory of constructed emotion: an active inference account of interoception and categorization
Barrett, L. F. (2017) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsx060 · Cited by 950 · see citing works
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Adolphs, R. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05445.x · Cited by 836 · see citing works
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Izquierdo, A., Brigman, J. L., Radke, A. K., Rudebeck, P. H., & Holmes, A. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2016.03.021 · Cited by 670 · see citing works
The ecology of human fear: survival optimization and the nervous system
Mobbs, D., Hagan, C. C., Dalgleish, T., Silston, B., & Prévost, C. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00055 · Cited by 498 · see citing works
Schott, B. H., Minuzzi, L., Krebs, R. M., Elmenhorst, D., Lang, M., Winz, O. H., Seidenbecher, C. I., Coenen, H. H., Heinze, H.-J., Zilles, K., et al. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2058-08.2008 · Cited by 496 · see citing works
Fear, faces, and the human amygdala
Adolphs, R. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.06.006 · Cited by 502 · see citing works
Self-citationGujar, N., Yoo, S.-S., Hu, P., & Walker, M. P. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3220-10.2011 · Cited by 491 · 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
Self-citationRubia, K. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.09.023 · Cited by 440 · see citing works
From Fear to Safety and Back: Reversal of Fear in the Human Brain
Schiller, D., Levy, I., Niv, Y., LeDoux, J. E., & Phelps, E. A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2265-08.2008 · Cited by 429 · see citing works
Gläscher, J., Hampton, A. N., & O'Doherty, J. P. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn098 · Cited by 387 · see citing works
Self-citationRudebeck, P. H., & Murray, E. A. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.049 · Cited by 405 · see citing works
Finger, E. C., Marsh, A. A., Mitchell, D. G., Reid, M. E., Sims, C., Budhani, S., Kosson, D. S., Chen, G., Towbin, K. E., Leibenluft, E., et al. (2008) · Archives of General Psychiatry · doi:10.1001/archpsyc.65.5.586 · Cited by 365 · see citing works
Emotion, decision making, and the amygdala.
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Maier, S. U., Makwana, A. B., & Hare, T. A. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.005 · Cited by 270 · see citing works
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Voos, A. C., Pelphrey, K. A., & Kaiser, M. D. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss009 · Cited by 205 · see citing works
Tsuchida, A., Doll, B. B., & Fellows, L. K. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1958-10.2010 · Cited by 188 · see citing works
“…reversal learning tasks, impaired performance not restricted to the reversal phase has also been observed in patients with amygdala damage (Hampton et al., 2007), patients with major depressive disorder (Murphy et al., 2003), and healthy subjects administered a central serotonin reuptake…”
BackgroundBasolateral amygdala to orbitofrontal cortex projections enable cue-triggered reward expectations
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Rudebeck, P. H., & Murray, E. A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2272-08.2008 · Cited by 148 · see citing works
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Boes, A. D., Mehta, S., Rudrauf, D., Van Der Plas, E., Grabowski, T., Adolphs, R., & Nopoulos, P. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsr047 · Cited by 23 · see citing works
Self-citationColas, J. T., O’Doherty, J. P., & Grafton, S. T. (2024) · PLOS Computational Biology · doi:10.1371/journal.pcbi.1011950 · Cited by 6 · see citing works
Self-citation
- Authors
- Hampton, A. N., Adolphs, R., Tyszka, J. M., & O'Doherty, J. P.
- Affiliations
- California Institute of Technology (US)
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2007-08
- Volume
- 55
- Issue
- 4
- Pages
- 545-555
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2020628123
- Cited by
- 213
- References
- 39
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 12 · 2023: 6 · 2022: 11 · 2021: 8 · 2020: 9 · 2019: 6 · 2018: 10 · 2017: 9 · 2016: 18 · 2015: 15 · 2014: 10 · 2013: 14 · 2012: 13
- FWCI
- 6.52
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- amygdala, prefrontal cortex, ventromedial prefrontal cortex, reward anticipation, behavioral choice, reversal learning, amygdala lesions, decision-making, reward learning
- MeSH terms
- Adult, Amygdala, Attention, Brain Injuries, Brain Mapping, Choice Behavior, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Middle Aged, Neuropsychological Tests, Oxygen, Reward, Time Factors, Prefrontal Cortex
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