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Psychopharmacology

, Volume 179, Issue 3, pp 587–596 | Cite as

Differential involvement of serotonin and dopamine systems in cost-benefit decisions about delay or effort

  • F. Denk
  • M. E. Walton
  • K. A. Jennings
  • T. Sharp
  • M. F. S. Rushworth
  • D. M. Bannerman
Original Investigation

Abstract

Rationale

Although tasks assessing the role of dopamine in effort-reward decisions are similar to those concerned with the role of serotonin in impulsive choice in that both require analysis of the costs and benefits of possible actions, they have never been directly compared.

Objectives

This study investigated the involvement of serotonin and dopamine in two cost-benefit paradigms, one in which the cost was delay and the other in which it was physical effort.

Methods

Sixteen rats were trained on a T-maze task in which they chose between high and low reward arms. In one version, the high reward arm was obstructed by a barrier, in the other, delivery of the high reward was delayed by 15 s. Serotonin and dopamine function were manipulated using systemic pCPA and haloperidol injections, respectively.

Results

Haloperidol-treated rats were less inclined either to exert more effort or to countenance a delay for a higher reward. pCPA had no effect on the performance of the rats on the effortful task, but significantly increased the rats’ preference for an immediate but smaller reward. All animals (drug treated and controls) chose the high reward arm on the majority of trials when the delay or effort costs were matched in both high and low reward arms.

Conclusion

A dissociation was found between the neurotransmitter systems involved in different types of cost-benefit decision making. While dopaminergic systems were required for decisions about both effort and delay, serotonergic systems were only needed for the latter.

Keywords

Cost-benefit evaluation Decision making Rat Effort Impulsivity Serotonin Dopamine Cingulate Nucleus accumbens 

Notes

Acknowledgements

This study was supported by the MRC, with additional support from the Wellcome Trust (M.E.W.). D.B. was supported by a Wellcome Trust grant to J.N.P. Rawlins. The support and encouragement of J.N.P. Rawlins is gratefully acknowledged. Treatment and care of the animals was in accordance with the Principles of laboratory animal care and the United Kingdom Animals Scientific Procedures Act (1986) under project licence number PPL 30/1505 and personal licenses held by the authors.

References

  1. Aberman JE, Salamone JD (1999) Nucleus accumbens dopamine depletions make rats more sensitive to high ratio requirements but do not impair primary food reinforcements. Neuroscience 92:545–552CrossRefGoogle Scholar
  2. Bechara A, Damasio AR, Damasio H, Anderson SW (1994) Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50:7–15CrossRefGoogle Scholar
  3. Bizot JC, Thiebot MH, Le Bihan C, Soubrie P, Simon P (1988) Effects of imipramine-like drugs and serotonin uptake blockers on delay of reward in rats. Possible implication in the behavioral mechanism of action of antidepressants. J Pharmacol Exp Ther 246:1144–1151PubMedGoogle Scholar
  4. Bizot J, Le Bihan C, Puech AJ, Hamon M, Thiebot M (1999) Serotonin and tolerance to delay of reward in rats. Psychopharmacology 146:400–412PubMedGoogle Scholar
  5. Cardinal RN, Pennicott DR, Sugathapala CL, Robbins TW, Everitt BJ (2001) Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science 292:2499–2501CrossRefGoogle Scholar
  6. Castro E, Tordera RM, Hughes ZA, Pei Q, Sharp T (2003) Use of Arc expression as a molecular marker of increased postsynaptic 5-HT function after SSRI/5-HT1A receptor antagonist co-administration. J Neurochem 85:1480–1487CrossRefGoogle Scholar
  7. Cole BJ, Robbins TW (1989) Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi on performance of a 5-choice serial reaction time task in rats: implications for theories of selective attention and arousal. Behav Brain Res 33:165–179PubMedGoogle Scholar
  8. Correa M, Carlson BB, Wisniecki A, Salamone JD (2002) Nucleus accumbens dopamine and work requirements on interval schedules. Behav Brain Res 137:179–187CrossRefGoogle Scholar
  9. Cousins MS, Salamone JD (1994) Nucleus accumbens dopamine depletions in rats affect relative response allocation in a novel cost/benefit procedure. Pharmacol Biochem Behav 49:85–91CrossRefGoogle Scholar
  10. Cousins MS, Atherton A, Turner L, Salamone JD (1996) Nucleus accumbens dopamine depletions alter relative response allocation in a T-maze cost/benefit task. Behav Brain Res 74:189–197CrossRefGoogle Scholar
  11. Evenden JL (1999) Varieties of impulsivity. Psychopharmacology 146:348–361PubMedGoogle Scholar
  12. Evenden JL, Ryan CN (1996) The pharmacology of impulsive behaviour in rats: the effects of drugs on response choice with varying delays of reinforcement. Psychopharmacology 128:161–170CrossRefGoogle Scholar
  13. Evenden JL, Ryan CN (1999) The pharmacology of impulsive behaviour in rats VI: the effects of ethanol and selective serotonergic drugs on response choice with varying delays of reinforcement. Psychopharmacology 146:413–421PubMedGoogle Scholar
  14. Hajos M, Sharp T (1996) A 5-hydroxytryptamine lesion markedly reduces the incidence of burst-firing dorsal raphe neurones in the rat. Neurosci Lett 204:161–164CrossRefGoogle Scholar
  15. Hajos M, Richards CD, Szekely AD, Sharp T (1998) An electrophysiological and neuroanatomical study of the medial prefrontal cortical projection to the midbrain raphe nuclei in the rat. Neuroscience 87:95–108CrossRefGoogle Scholar
  16. Horvitz JC, Ettenberg A (1988) Haloperidol blocks the response-reinstating effects of food reward: a methodology for separating neuroleptic effects on reinforcement and motor processes. Pharmacol Biochem Behav 31:861–865CrossRefGoogle Scholar
  17. Ishiwari K, Weber SM, Mingote S, Correa M, Salamone JD (2004) Accumbens dopamine and the regulation of effort in food-seeking behavior: modulation of work output by different ratio or force requirements. Behav Brain Res 151:83–91CrossRefGoogle Scholar
  18. Jakala P, Sirvio J, Jolkkonen J, Riekkinen P Jr, Acsady L, Riekkinen P (1992) The effects of p-chlorophenylalanine-induced serotonin synthesis inhibition and muscarinic blockade on the performance of rats in a 5-choice serial reaction time task. Behav Brain Res 51:29–40PubMedGoogle Scholar
  19. Kheramin S, Body S, Mobini S, Ho MY, Velazquez-Martinez DN, Bradshaw CM, Szabadi E, Deakin JF, Anderson IM (2002) Effects of quinolinic acid-induced lesions of the orbital prefrontal cortex on inter-temporal choice: a quantitative analysis. Psychopharmacology 165:9–17CrossRefGoogle Scholar
  20. Liao RM, Fowler SC (1990) Haloperidol produces within-session increments in operant response duration in rats. Pharmacol Biochem Behav 36:191–201CrossRefGoogle Scholar
  21. London ED, Ernst M, Grant S, Bonson K, Weinstein A (2000) Orbitofrontal cortex and human drug abuse: functional imaging. Cereb Cortex 10:334–342CrossRefPubMedGoogle Scholar
  22. Manes F, Sahakian B, Clark L, Rogers R, Antoun N, Aitken M, Robbins T (2002) Decision-making processes following damage to the prefrontal cortex. Brain 125:624–639CrossRefGoogle Scholar
  23. McQuade R, Sharp T (1995) Release of cerebral 5-hydroxytryptamine evoked by electrical stimulation of the dorsal and median raphe nuclei: effect of a neurotoxic amphetamine. Neuroscience 68:1079–1088CrossRefGoogle Scholar
  24. Mobini S, Chiang TJ, Ho MY, Bradshaw CM, Szabadi E (2000a) Comparison of the effects of clozapine, haloperidol, chlorpromazine and d-amphetamine on performance on a time-constrained progressive ratio schedule and on locomotor behaviour in the rat. Psychopharmacology 152:47–54CrossRefPubMedGoogle Scholar
  25. Mobini S, Chiang TJ, Ho MY, Bradshaw CM, Szabadi E (2000b) Effects of central 5-hydroxytryptamine depletion on sensitivity to delayed and probabilistic reinforcement. Psychopharmacology 152:390–397CrossRefGoogle Scholar
  26. Mobini S, Body S, Ho MY, Bradshaw CM, Szabadi E, Deakin JF, Anderson IM (2002) Effects of lesions of the orbitofrontal cortex on sensitivity to delayed and probabilistic reinforcement. Psychopharmacology 160:290–298CrossRefGoogle Scholar
  27. Murphy FC, Rubinsztein JS, Michael A, Rogers RD, Robbins TW, Paykel ES, Sahakian BJ (2001) Decision-making cognition in mania and depression. Psychol Med 31:679–693CrossRefGoogle Scholar
  28. Peterson JD, Wolf ME, White FJ (2003) Impaired DRL 30 performance during amphetamine withdrawal. Behav Brain Res 143:101–108CrossRefGoogle Scholar
  29. Rahman S, Sahakian BJ, Hodges JR, Rogers RD, Robbins TW (1999) Specific cognitive deficits in mild frontal variant frontotemporal dementia. Brain 122(Pt 8):1469–1493CrossRefGoogle Scholar
  30. Rahman SJ, Sahakian BJ, Cardinal RN, Rogers RD, Robbins TW (2001) Decision making and neuropsychiatry. Trends Cogn Sci 5:271–277CrossRefGoogle Scholar
  31. Rogers RD, Everitt BJ, Baldacchino A, Blackshaw AJ, Swainson R, Wynne K, Baker NB, Hunter J, Carthy T, Booker E, London M, Deakin JF, Sahakian BJ, Robbins TW (1999) Dissociable deficits in the decision-making cognition of chronic amphetamine abusers, opiate abusers, patients with focal damage to prefrontal cortex, and tryptophan-depleted normal volunteers: evidence for monoaminergic mechanisms. Neuropsychopharmacology 20:322–339CrossRefPubMedGoogle Scholar
  32. 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 28:153–162CrossRefPubMedGoogle Scholar
  33. Salamone JD, Correa M (2002) Motivational views of reinforcement: implications for understanding the behavioral functions of nucleus accumbens dopamine. Behav Brain Res 137:3–25CrossRefGoogle Scholar
  34. Salamone JD, Steinpreis RE, McCullough LD, Smith P, Grebel D, Mahan K (1991) Haloperidol and nucleus accumbens dopamine depletion suppress lever pressing for food but increase free food consumption in a novel food choice procedure. Psychopharmacology 104:515–521PubMedGoogle Scholar
  35. Salamone JD, Cousins MS, Bucher S (1994) Anhedonia or anergia? Effects of haloperidol and nucleus accumbens dopamine depletion on instrumental response selection in a T-maze cost/benefit procedure. Behav Brain Res 65:221–229CrossRefPubMedGoogle Scholar
  36. Salamone JD, Wisniecki A, Carlson BB, Correa M (2001) Nucleus accumbens dopamine depletions make animals highly sensitive to high fixed ratio requirements but do not impair primary food reinforcement. Neuroscience 105:863–870CrossRefGoogle Scholar
  37. Sokolowski JD, Conlan AN, Salamone JD (1998) A microdialysis study of nucleus accumbens core and shell dopamine during operant responding in the rat. Neuroscience 86:1001–1009CrossRefGoogle Scholar
  38. Thiebot MH, Le Bihan C, Soubrie P, Simon P (1985) Benzodiazepines reduce the tolerance to reward delay in rats. Psychopharmacology 86:147–152CrossRefGoogle Scholar
  39. Wade TR, de Wit H, Richards JB (2000) Effects of dopaminergic drugs on delayed reward as a measure of impulsive behavior in rats. Psychopharmacology 150:90–101CrossRefPubMedGoogle Scholar
  40. Walton ME, Bannerman DM, Rushworth MF (2002) The role of rat medial frontal cortex in effort-based decision making. J Neurosci 22:10996–11003PubMedGoogle Scholar
  41. Walton ME, Bannerman DM, Alterescu K, Rushworth MF (2003) Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions. J Neurosci 23:6475–6479PubMedGoogle Scholar
  42. Walton ME, Croxson I-L, Rushworth MFS, Bannerman DM (2004) The Mesocortical dopamine projection to anterior cingulate cortex plays no role in guiding effort-related decisions. Behav Neurosci, in pressGoogle Scholar
  43. Wise RA (1982) Neuroleptics and operant behavior: the anhedonia hypothesis. Behav Brain Sci 5:39–87Google Scholar
  44. Wise RA, Bozarth MA (1987) A psychomotor stimulant theory of addiction. Psychol Rev 94:469–492CrossRefPubMedGoogle Scholar
  45. Wogar MA, Bradshaw CM, Szabadi E (1993) Effect of lesions of the ascending 5-hydroxytryptaminergic pathways on choice between delayed reinforcers. Psychopharmacology 111:239–243PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • F. Denk
    • 1
  • M. E. Walton
    • 1
  • K. A. Jennings
    • 2
  • T. Sharp
    • 2
  • M. F. S. Rushworth
    • 1
  • D. M. Bannerman
    • 1
  1. 1.Department of Experimental PsychologyUniversity of OxfordOxfordUK
  2. 2.Department of PharmacologyUniversity of OxfordOxfordUK

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