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Edited by John P. O’Doherty, California Institute of Technology, Pasadena, CA, and accepted by the Editorial Board June 24, 2014 (received for review December 18, 2013)
Significance
Organisms must learn adaptively about environmental cue–outcome associations to survive. Studies in nonhuman primates suggest that a small phylogenetically conserved brain structure, the habenula, encodes the values of cues previously paired with aversive outcomes. However, such a role for the habenula has never been demonstrated in humans. We establish that the habenula encodes associations with aversive outcomes in humans, specifically that it tracks the dynamically changing negative values of cues paired with painful electric shocks, consistent with a role in learning. Importantly, habenula responses predicted the extent to which individuals withdrew from or approached negative and positive cues, respectively. These results suggest that the habenula plays a central role in driving aversively motivated learning and behavior in humans.
Abstract
Learning what to approach, and what to avoid, involves assigning value to environmental cues that predict positive and negative events. Studies in animals indicate that the lateral habenula encodes the previously learned negative motivational value of stimuli. However, involvement of the habenula in dynamic trial-by-trial aversive learning has not been assessed, and the functional role of this structure in humans remains poorly characterized, in part, due to its small size. Using high-resolution functional neuroimaging and computational modeling of reinforcement learning, we demonstrate positive habenula responses to the dynamically changing values of cues signaling painful electric shocks, which predict behavioral suppression of responses to those cues across individuals. By contrast, negative habenula responses to monetary reward cue values predict behavioral invigoration. Our findings show that the habenula plays a key role in an online aversive learning system and in generating associated motivated behavior in humans.
Footnotes
- ↵1To whom correspondence may be addressed. Email: rebecca.lawson{at}ucl.ac.uk or j.roiser{at}ucl.ac.uk.
Author contributions: R.P.L., B.S., R.J.D., P.D., and J.P.R. designed research; R.P.L. and E.L. performed research; R.P.L. and B.S. analyzed data; R.P.L., B.S., R.J.D., P.D., N.W., and J.P.R. wrote the paper; A.L. and N.W. developed imaging methods; and J.P.R. conceived the study.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. J.P.O. is a guest editor invited by the Editorial Board.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1323586111/-/DCSupplemental.
Freely available online through the PNAS open access option.
- Rebecca P. Lawsona,b,1,
- Ben Seymourc,d,
- Eleanor Lohb,
- Antoine Luttib,e,
- Raymond J. Dolanb,
- Peter Dayanf,
- Nikolaus Weiskopfb, and
- Jonathan P. Roisera,1
- aInstitute of Cognitive Neuroscience, University College London, London WC1N 3AR, United Kingdom;
- bWellcome Trust Centre for Neuroimaging, University College London, London WC1N 3BG, United Kingdom;
- cComputational and Biological Learning Laboratory, Department of Engineering, University of Cambridge, Cambridge CB2 1PZ, United Kingdom;
- dCenter for Information and Neural Networks, National Institute for Information and Communications Technology, Osaka 565-0871, Japan;
- eLaboratoire de Recherche en Neuroimagerie, Département des Neurosciences Cliniques, Centre Hospitalier Universitaire Vaudois, Université de Lausanne, 1011 Lausanne, Switzerland; and
- fGatsby Computational Neuroscience Unit, University College London, London WC1N 3AR, United Kingdom
Edited by John P. O’Doherty, California Institute of Technology, Pasadena, CA, and accepted by the Editorial Board June 24, 2014 (received for review December 18, 2013)
Significance
Organisms must learn adaptively about environmental cue–outcome associations to survive. Studies in nonhuman primates suggest that a small phylogenetically conserved brain structure, the habenula, encodes the values of cues previously paired with aversive outcomes. However, such a role for the habenula has never been demonstrated in humans. We establish that the habenula encodes associations with aversive outcomes in humans, specifically that it tracks the dynamically changing negative values of cues paired with painful electric shocks, consistent with a role in learning. Importantly, habenula responses predicted the extent to which individuals withdrew from or approached negative and positive cues, respectively. These results suggest that the habenula plays a central role in driving aversively motivated learning and behavior in humans.
Abstract
Learning what to approach, and what to avoid, involves assigning value to environmental cues that predict positive and negative events. Studies in animals indicate that the lateral habenula encodes the previously learned negative motivational value of stimuli. However, involvement of the habenula in dynamic trial-by-trial aversive learning has not been assessed, and the functional role of this structure in humans remains poorly characterized, in part, due to its small size. Using high-resolution functional neuroimaging and computational modeling of reinforcement learning, we demonstrate positive habenula responses to the dynamically changing values of cues signaling painful electric shocks, which predict behavioral suppression of responses to those cues across individuals. By contrast, negative habenula responses to monetary reward cue values predict behavioral invigoration. Our findings show that the habenula plays a key role in an online aversive learning system and in generating associated motivated behavior in humans.
- high-resolution fMRI
- conditioned behavior
- pallidum
Footnotes
- ↵1To whom correspondence may be addressed. Email: rebecca.lawson{at}ucl.ac.uk or j.roiser{at}ucl.ac.uk.
Author contributions: R.P.L., B.S., R.J.D., P.D., and J.P.R. designed research; R.P.L. and E.L. performed research; R.P.L. and B.S. analyzed data; R.P.L., B.S., R.J.D., P.D., N.W., and J.P.R. wrote the paper; A.L. and N.W. developed imaging methods; and J.P.R. conceived the study.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. J.P.O. is a guest editor invited by the Editorial Board.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1323586111/-/DCSupplemental.
Freely available online through the PNAS open access option.
Habenula encodes negative motivational value
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