The habenula encodes negative motivational value associated with primary punishment in humans

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 32, 2014, Pages 11858-11863

  Lawson, Rebecca P ^a,b   Seymour, Ben ^c,d   Loh, Eleanor ^b   Lutti, Antoine ^b,e   Dolan, Raymond J ^b   Dayan, Peter ^f   Weiskopf, Nikolaus ^b   Roiser, Jonathan P ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d NATIONAL INSTITUTE OF INFORMATION AND COMMUNICATIONS TECHNOLOGY   (Japan)

^e UNIVERSITY OF LAUSANNE   (Switzerland)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Conditioned behavior; High resolution fMRI; Pallidum

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; ASSOCIATION; BOLD SIGNAL; CORPUS STRIATUM; ELECTRIC SHOCK; FEMALE; FUNCTIONAL NEUROIMAGING; GLOBUS PALLIDUS; HABENULA; HEMISPHERIC DOMINANCE; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; NEGATIVE MOTIVATIONAL VALUE; NORMAL HUMAN; PRIORITY JOURNAL; PUNISHMENT; REINFORCEMENT; THALAMUS;

CONDITIONED BEHAVIOR; HIGH-RESOLUTION FMRI; PALLIDUM;

ADULT; ANIMALS; CONDITIONING (PSYCHOLOGY); CUES; FEMALE; FUNCTIONAL NEUROIMAGING; HABENULA; HUMANS; LEARNING; MAGNETIC RESONANCE IMAGING; MALE; MOTIVATION; PUNISHMENT; REINFORCEMENT (PSYCHOLOGY); SPECIES SPECIFICITY; YOUNG ADULT;

EID: 84905969306     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1323586111     Document Type: Article

References (46)

1. Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275(5306):1593-1599
2. Matsumoto M, Hikosaka O (2007) Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447(7148):1111-1115
3. Estes WK, Skinner BF (1941) Some quantitative properties of anxiety. J Exp Psychol 29(5):390-400
4. Hong S, Hikosaka O (2008) The globus pallidus sends reward-related signals to the lateral habenula. Neuron 60(4):720-729
5. Hikosaka O (2010) The habenula: From stress evasion to value-based decision-making. Nat Rev Neurosci 11(7):503-513
6. Stamatakis AM, Stuber GD (2012) Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance. Nat Neurosci 15(8):1105-1107
7. Sartorius A, et al. (2010) Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient. Biol Psychiatry 67(2):e9-e11
8. Sartorius A, Henn FA (2007) Deep brain stimulation of the lateral habenula in treatment resistant major depression. Med Hypotheses 69(6):1305-1308
9. Lawson RP, Drevets WC, Roiser JP (2013) Defining the habenula in human neuroimaging studies. Neuroimage 64:722-727
10. Ide JS, Li C-SR (2011) Error-related functional connectivity of the habenula in humans. Front Hum Neurosci 5:25
11. Ullsperger M, von Cramon DY (2003) Error monitoring using external feedback: Specific roles of the habenular complex, the reward system, and the cingulate motor area revealed by functional magnetic resonance imaging. J Neurosci 23(10): 4308-4314
12. Shelton L, et al. (2012) Mapping pain activation and connectivity of the human habenula. J Neurophysiol 107(10):2633-2648
13. Seymour B, et al. (2004) Temporal difference models describe higher-order learning in humans. Nature 429(6992):664-667
14. O'Doherty JP, Dayan P, Friston K, Critchley H, Dolan RJ (2003) Temporal difference models and reward-related learning in the human brain. Neuron 38(2):329-337
15. Haber SN, Knutson B (2010) The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology 35(1):4-26
16. Bitsios P, Szabadi E, Bradshaw CM (2004) The fear-inhibited light reflex: Importance of the anticipation of an aversive event. Int J Psychophysiol 52(1):87-95
17. Bromberg-Martin ES, Matsumoto M, Hong S, Hikosaka O (2010) A pallidus-habenuladopamine pathway signals inferred stimulus values. J Neurophysiol 104(2):1068-1072
18. Shabel SJ, Proulx CD, Trias A, Murphy RT, Malinow R (2012) Input to the lateral habenula from the basal ganglia is excitatory, aversive, and suppressed by serotonin. Neuron 74(3):475-481
19. Matsumoto M, Hikosaka O (2009) Representation of negative motivational value in the primate lateral habenula. Nat Neurosci 12(1):77-84
20. Salas R, Baldwin P, de Biasi M, Montague PR (2010) BOLD Responses to Negative Reward Prediction Errors in Human Habenula. Front Hum Neurosci 4:36
21. Delgado MR, Labouliere CD, Phelps EA (2006) Fear of losing money? Aversive conditioning with secondary reinforcers. Soc Cogn Affect Neurosci 1(3):250-259
22. Stopper CM, Floresco SB (2014) What's better for me? Fundamental role for lateral habenula in promoting subjective decision biases. Nat Neurosci 17(1):33-35
23. Bianco IH, Wilson SW (2009) The habenular nuclei: A conserved asymmetric relay station in the vertebrate brain. Philos Trans R Soc Lond B Biol Sci 364(1519): 1005-1020
24. Amo R, et al. (2010) Identification of the zebrafish ventral habenula as a homolog of the mammalian lateral habenula. J Neurosci 30(4):1566-1574
25. Lee HJ, et al. (2005) Role of amygdalo-nigral circuitry in conditioning of a visual stimulus paired with food. J Neurosci 25(15):3881-3888
26. Garrison J, Erdeniz B, Done J (2013) Prediction error in reinforcement learning: A meta-analysis of neuroimaging studies. Neurosci Biobehav Rev 37(7):1297-1310
27. MiladMR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420(6911):70-74
28. Phelps EA, Delgado MR, Nearing KI, LeDoux JE (2004) Extinction learning in humans: Role of the amygdala and vmPFC. Neuron 43(6):897-905
29. Roiser JP, et al. (2009) The effects of tryptophan depletion on neural responses to emotional words in remitted depression. Biol Psychiatry 66(5):441-450
30. Savitz JB, et al. (2011) Habenula volume in bipolar disorder and major depressive disorder: A high-resolution magnetic resonance imaging study. Biol Psychiatry 69(4): 336-343
31. Li B, et al. (2011) Synaptic potentiation onto habenula neurons in the learned helplessness model of depression. Nature 470(7335):535-539
32. Carlson PJ, et al. (2013) Neural correlates of rapid antidepressant response to ketamine in treatment-resistant unipolar depression: a preliminary positron emission tomography study. Biol Psychiatry 73(12):1213-1221
33. Vlaev I, Seymour B, Dolan RJ, Chater N (2009) The price of pain and the value of suffering. Psychol Sci 20(3):309-317
34. Lutti A, Thomas DL, Hutton C, Weiskopf N (2013) High-resolution functional MRI at 3 T: 3D/2D echo-planar imaging with optimized physiological noise correction. Magn Reson Med 69(6):1657-1664
35. Hutton C, et al. (2011) The impact of physiological noise correction on fMRI at 7 T. Neuroimage 57(1):101-112
36. Deichmann R, Schwarzbauer C, Turner R (2004) Optimisation of the 3D MDEFT sequence for anatomical brain imaging: Technical implications at 1.5 and 3 T. Neuroimage 21(2):757-767
37. Hutton C, et al. (2002) Image distortion correction in fMRI: A quantitative evaluation. Neuroimage 16(1):217-240
38. Seymour B, Daw N, Dayan P, Singer T, Dolan R (2007) Differential encoding of losses and gains in the human striatum. J Neurosci 27(18):4826-4831
39. Seymour B, et al. (2005) Opponent appetitive-aversive neural processes underlie predictive learning of pain relief. Nat Neurosci 8(9):1234-1240
40. Brett M, Anton J-L, Valabregue R, Poline J-B (2002) Region of interest analysis using an SPM toolbox. 8th International Conference on Functional Mapping of the Human Brain. Available on CD-ROM in NeuroImage 16(2) (abstr
41. Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38(1):95-113
42. Friston KJ, et al. (1997) Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6(3):218-229
43. Mai J, Paxinos G, Voss T (2008) Atlas of the Human Brain (Academic, San Diego), 3rd Ed
44. O'Doherty J, et al. (2004) Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304(5669):452-454
45. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19(3):1233-1239
46. Raghunathan TE, Rosenthal R, Rubin DB (1996) Comparing correlated but nonoverlapping correlations. Psychol Methods 1(2):178-183.