Serotonin and aversive pavlovian control of instrumental behavior in humans

Journal of Neuroscience

Volumn 33, Issue 48, 2013, Pages 18932-18939

  Geurts, Dirk E M ^a   Huys, Quentin J M ^b,c,d   den Ouden, Hanneke E M ^a   Cools, Roshan ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d University Hospital of Psychiatry Zurich   (Switzerland)

Author keywords

Aversive; Inhibition; Instrumental; Pavlovian; Serotonin; Tryptophan depletion

Indexed keywords

SEROTONIN; TRYPTOPHAN; AMINO ACID;

ADULT; AMINO ACID DEFICIENCY; APPETITE; ARTICLE; AVERSIVE BEHAVIOR; CONDITIONING; FEMALE; HUMAN; HUMAN EXPERIMENT; INSTRUMENTAL CONDITIONING; MALE; MOOD; NORMAL HUMAN; PAVLOVIAN CONDITIONING; PRIORITY JOURNAL; PSYCHOMETRY; QUESTIONNAIRE; TASK PERFORMANCE; TRAINING; ADOLESCENT; AFFECT; ASSOCIATION; BEHAVIOR; BLOOD; CONDITIONED REFLEX; DECISION MAKING; DEFICIENCY; METABOLISM; NEUROPSYCHOLOGICAL TEST; PERSONALITY TEST; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; REINFORCEMENT; SEROTONINERGIC NERVE CELL; STATISTICAL ANALYSIS; YOUNG ADULT;

ADOLESCENT; ADULT; AFFECT; AMINO ACIDS; APPETITE; BEHAVIOR; CONDITIONING, CLASSICAL; CUES; DATA INTERPRETATION, STATISTICAL; DECISION MAKING; FEMALE; HUMANS; MALE; NEUROPSYCHOLOGICAL TESTS; PERSONALITY TESTS; PSYCHOMETRICS; PSYCHOMOTOR PERFORMANCE; REINFORCEMENT (PSYCHOLOGY); SEROTONERGIC NEURONS; SEROTONIN; TRYPTOPHAN; YOUNG ADULT;

EID: 84888257227     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2749-13.2013     Document Type: Article

References (52)

1. Beck AT, Steer RA, Ball R, RanieriW (1996) Comparison of beck depression inventories-IA and-II in psychiatric outpatients. J Pers Assess 67:588-597. CrossRef Medline
2. Bond A, Lader M (1974) The use of analogue scales in rating subjective feelings. Br J Med Psychol 47:211-218. CrossRef
3. Boureau YL, Dayan P (2011) Opponency revisited: competition and cooperation between dopamine and serotonin. Neuropsychopharmacology 36:74-97. CrossRef Medline
4. Bromberg-Martin ES, Hikosaka O, Nakamura K (2010) Coding of task reward value in the dorsal raphe nucleus. J Neurosci 30:6262-6272. CrossRef Medline
5. Carver CS, White TL (1994) Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: the BIS/ BAS scales. J Pers Soc Psychol 67:319. CrossRef
6. Cools R, Blackwell A, Clark L, Menzies L, Cox S, Robbins TW (2005) Tryptophan depletion disrupts the motivational guidance of goal-directed behavior as a function of trait impulsivity. Neuropsychopharmacology 30: 1362-1373. CrossRef Medline
7. Cools R, Roberts AC, Robbins TW (2008a) Serotoninergic regulation of emotional and behavioral control processes. Trends Cogn Sci 12:31-40. CrossRef Medline
8. Cools R, Robinson OJ, Sahakian B (2008) Acute tryptophan depletion in healthy volunteers enhances punishment prediction but does not affect reward prediction. Neuropsychopharmacology 33:2291-2299. CrossRef Medline
9. Cools R, Nakamura K, Daw ND (2011) Serotonin and dopamine: unifying affective, activational, and decision functions. Neuropsychopharmacology 36:98-113. CrossRef Medline
10. Crockett MJ, Clark L, RobbinsTW (2009) Reconciling the role of serotonin in behavioral inhibition and aversion: acute tryptophan depletion abolishes punishment-induced inhibition in humans. J Neurosci 29:11993-11999. CrossRef Medline
11. Crockett MJ, Clark L, Roiser JP, Robinson OJ, Cools R, Chase HW, Ouden Hd, Apergis-Schoute A, Campbell-Meiklejohn D, Campbell-Meikeljohn D, Seymour B, Sahakian BJ, Rogers RD, Robbins TW (2012) Converging evidence for central 5-HT effects in acute tryptophan depletion. Mol Psychiatry 17:121-123. CrossRef Medline
12. Crockett MJ, Clark L, Apergis-Schoute AM, Morein-Zamir S, Robbins TW (2012) Serotonin modulates the effects of Pavlovian aversive predictions on response vigor. Neuropsychopharmacology 37:2244-2252. CrossRef Medline
13. Daw ND, Kakade S, Dayan P (2002) Opponent interactions between serotonin and dopamine. Neural Netw 15:603-616. CrossRef Medline
14. Dayan P, Huys QJ (2008) Serotonin, inhibition, and negative mood. PLoS Comput Biol 4:e4. CrossRef Medline
15. Dayan P, Huys QJ (2009) Serotonin in affective control. Annu Rev Neurosci 32:95-126. CrossRef Medline
16. Dayan P, Niv Y, Seymour B, Daw ND (2006) The misbehavior of value and the discipline of the will. Neural Netw 19:1153-1160. CrossRef Medline
17. Deakin JF (1983) Roles of serotonergic systems in escape, avoidance and other behaviors. In: Theory in Psychopharmacology (S C, ed). London and New York: Academic.
18. Deakin JF, Graeff FG (1991) 5-HT and mechanisms of defence. J Psychopharmacol 5:305-315. CrossRef Medline
19. Eysenck HJ, Eysenck SBG (1975) Manual of the Eysenck Personality Questionnaire. London: Hodder and Stoughton.
20. Fekkes D, van Dalen A, Edelman M, Voskuilen A (1995) Validation of the determination of amino acids in plasma by high-performance liquid chromatography using automated pre-column derivatization with o-phthaldialdehyde. J Chromatogr B Biomed Appl 669:177-186. CrossRef Medline
21. Fernstrom JD, Wurtman RJ (1972) Brain serotonin content: physiological regulation by plasma neutral amino acids. Science 178:414-416. CrossRef Medline
22. Geurts DEM, Huys QJM, Ouden den HEM, Cools R (2013) Aversive Pavlovian control of instrumental behavior in humans. J Cogn Neurosci 25:1428-1441. CrossRef Medline
23. Graeff FG, Guimarães FS, De Andrade TG, Deakin JF (1996) Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 54:129-141. CrossRef Medline
24. Guitart-Masip M, Huys QJ, Fuentemilla L, Dayan P, Duzel E, Dolan RJ (2012) Go and no-go learning in reward and punishment: interactions between affect and effect. Neuroimage 62:154-166. CrossRef Medline
25. Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56-62. CrossRef Medline
26. Huys QJ, Cools R, Gölzer M, Friedel E, Heinz A, Dolan RJ, Dayan P (2011) Disentangling the roles of approach, activation and valence in instrumental and Pavlovian responding. PLoS Comput Biol 7:e1002028. CrossRef Medline
27. Huys QJ, Eshel N, O'Nions E, Sheridan L, Dayan P, Roiser JP (2012) Bonsai trees in your head: how the Pavlovian system sculpts goal-directed choices by pruning decision trees. PLoS Comput Biol 8:e1002410. CrossRef Medline
28. Kirby KN, Maraković NN (1996) Delay-discounting probabilistic rewards: rates decrease as amounts increase. Psychonomic Bull Rev 3:100-104. CrossRef
29. Kranz GS, Kasper S, Lanzenberger R (2010) Reward and the serotonergic system. Neuroscience 166:1023-1035. CrossRef Medline
30. Man MS, Mikheenko Y, Braesicke K, Cockcroft G, Roberts AC (2011) Serotonin at the level of the amygdala and orbitofrontal cortex modulates distinct aspects of positive emotion in primates. Int J Neuropsychopharmacol 15:91-105. CrossRef Medline
31. McNaughton N, Corr PJ (2004) Atwo-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neurosci Biobehav Rev 28: 285-305. CrossRef Medline
32. Miyazaki K, Miyazaki KW, Doya K (2012) The role of serotonin in the regulation of patience and impulsivity. Mol Neurobiol 45:213-224. CrossRef Medline
33. Nakamura K, Matsumoto M, Hikosaka O (2008) Reward-dependent modulation of neuronal activity in the primate dorsal raphe nucleus. J Neurosci 28:5331-5343. CrossRef Medline
34. Okada KI, Nakamura K, Kobayashi Y (2011) A neural correlate of predicted and actual reward-value information in monkey pedunculopontine tegmental and dorsal raphe nucleus during saccade tasks. Neural Plast 2011: 2011:579840. CrossRef Medline
35. Patton JH, Stanford MS, Barratt ES (1995) Factor structure of the Barratt impulsiveness scale. J Clin Psychol 51:768-774. CrossRef Medline
36. Pavlov IP (1927) Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex. London: Oxford UP.
37. Reilly JG, McTavish SF, Young AH (1997) Rapid depletion of plasma tryptophan: a review of studies and experimental methodology. J Psychopharmacol 11:381-392. CrossRef Medline
38. Robinson OJ, Sahakian BJ (2008) Recurrence in major depressive disorder: a neurocognitive perspective. Psychol Med 38:315-318. CrossRef Medline
39. Robinson OJ, Sahakian BJ (2009) Acute tryptophan depletion evokes negative mood in healthy females who have previously experienced concurrent negative mood and tryptophan depletion. Psychopharmacology 205: 227-235. CrossRef Medline
40. Robinson OJ, Cools R, Sahakian BJ (2012) Tryptophan depletion disinhibits punishment but not reward prediction: implications for resilience. Psychopharmacology 219:599-605. CrossRef Medline
41. Rogers RD, Tunbridge EM, Bhagwagar Z, Drevets WC, Sahakian BJ, Carter CS (2003) Tryptophan depletion alters the decision-making of healthy volunteers through altered processing of reward cues. Neuropsychopharmacology 28:153-162. CrossRef Medline
42. Saulin A, Savli M, Lanzenberger R (2012) Serotonin and molecular neuroimaging in humans using PET. Amino Acids 42:2039-2057. CrossRef Medline
43. Schmand B, Bakker D, Saan R, Louman J (1991) The Dutch reading test for adults: a measure of premorbid intelligence level. Tijdschrift voor Gerontologie en Geriatrie 22:15-19. Medline
44. Seymour B, Daw ND, Roiser JP, Dayan P, Dolan R (2012) Serotonin selectively modulates reward value in human decision-making. J Neurosci 32:5833-5842. CrossRef Medline
45. Soubrie P (1986) Reconciling the role of central serotonin neurons in human and animal behavior. Behav Brain Sci 9:319-335. CrossRef
46. Spielberger CD, Gorsuch RL, Lushene R, Vagg PR, Jacobs GA (1983) Manual for the state-trait anxiety inventory. Palo Alto, CA: Consluting Pscyhologists.
47. Thorndike EL (1911) Animal intelligence. New York: Macmillan.
48. Torrubia R, Ávila C, Moltó J, Caseras X (2001) The sensitivity to punishment and sensitivity to reward questionnaire (SPSRQ) as a measure of gray's anxiety and impulsivity dimensions. Pers Individ Diff 31:837-862. CrossRef
49. Tye NC, Everitt BJ, Iversen SD (1977) 5-hydroxytryptamine and punishment. Nature 268:741-743. CrossRef Medline
50. Watson D, Clark LA, TellegenA (1988) Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol 54:1063-1070. CrossRef Medline
51. Yin HH, Ostlund SB, Balleine BW (2008) Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of corticobasal ganglia networks. Eur J Neurosci 28:1437-1448. CrossRef Medline
52. Young SN, Smith SE, Pihl RO, Ervin FR (1985) Tryptophan depletion causes a rapid lowering of mood in normal males. Psychopharmacology 87:173-177. CrossRef Medline