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Modulation of Behavior by Expected Reward Magnitude Depends on Dopamine in the Dorsomedial Striatum

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Abstract

Reward-predictive cues are important to guide behavioral responding. In a series of experiments, we sought to characterize the role of dopamine in the dorsomedial striatum in modulation of reward-directed responding by visual cues. Different groups of rats subjected to infusion of 6-hydroxydopamine or vehicle into the posterior part of the dorsomedial striatum (pDMS) were tested in three experiments. In experiment 1, rats were examined in an operant task demanding a lever release response. In intact rats, reaction times of responding were reliably shorter on cued large reward trials than on cued small reward trials. Results showed that pDMS dopamine depletion impaired reward-dependent modulation of reaction times, if visual cues predict large versus small reward, but not if visual cues predict reward versus no reward. These observations suggest that dopamine signaling in the pDMS contributes to a process through which reward-directed responses become guided by cues associated with distinct reward magnitudes. Experiment 2 revealed that pDMS dopamine depletion did not compromise the acquisition of a conditional visual discrimination task in an operant box that required learning a rule of the type “if the cue light is bright press left lever for reward, if dim press right lever”. Furthermore, experiment 3 showed that pDMS dopamine depletion did not impair the acquisition of a cross maze task that required learning a visual cue discrimination strategy to obtain food reward. Together results of experiments 2 and 3 indicate that dopamine signaling in the pDMS does not subserve stimulus discrimination per se and stimulus-response learning.

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References

  • Adams S, Kesner RP, Ragozzino ME (2001) Role of the medial and lateral caudate-putamen in mediating an auditory conditional response association. Neurobiol Learn Mem 76(1):106–116

    Article  PubMed  CAS  Google Scholar 

  • Amalric M, Koob GF (1987) Depletion of dopamine in the caudate nucleus but not in nucleus accumbens impairs reaction-time performance in rats. J Neurosci 7(7):2129–2134

    PubMed  CAS  Google Scholar 

  • Aosaki T, Tsubokawa H, Ishida A, Watanabe K, Graybiel AM, Kimura M (1994) Responses of tonically active neurons in the primate’s striatum undergo systematic changes during behavioral sensorimotor conditioning. J Neurosci 14(6):3969–3984

    PubMed  CAS  Google Scholar 

  • Bailey KR, Mair RG (2006) The role of striatum in initiation and execution of learned action sequences in rats. J Neurosci 26(3):1016–1025

    Article  PubMed  CAS  Google Scholar 

  • Barnes TD, Kubota Y, Hu D, Jin DZ, Graybiel AM (2005) Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 437(7062):1158–1161

    Article  PubMed  CAS  Google Scholar 

  • Bloomfield TM (1967) Behavioral contrast and relative reinforcement frequency in two multiple schedules. J Exp Anal Behav 10(2):151–158

    Article  PubMed  CAS  Google Scholar 

  • Brasted PJ, Wise SP (2004) Comparison of learning-related neuronal activity in the dorsal premotor cortex and striatum. Eur J NeuroSci 19(3):721–740

    Article  PubMed  Google Scholar 

  • Brown VJ, Robbins TW (1991a) Simple and choice reaction time performance following unilateral striatal dopamine depletion in the rat. Brain 114:513–525

    Article  PubMed  Google Scholar 

  • Brown VJ, Robbins TW (1991b) Simple and choice reaction time performance following unilateral striatal dopamine depletion in the rat. Impaired motor readiness but preserved response preparation. Brain 114(Pt 1B):513–525

    Article  PubMed  Google Scholar 

  • Calaminus C, Hauber W (2007) Intact discrimination reversal learning but slowed responding to reward-predictive cues after dopamine D1 and D2 receptor blockade in the nucleus accumbens of rats. Psychopharmacology (Berl) 191(3):551–566

    Article  CAS  Google Scholar 

  • Colwill RM, Rescorla RA (1988) Associations between the discrimintaive stimulus and the reinforcer in instrumental learning. J Exp Psychol Anim Behav Process 14:155–164

    Article  Google Scholar 

  • Corbit LH, Janak PH (2007) Inactivation of the lateral but not medial dorsal striatum eliminates the excitatory impact of Pavlovian stimuli on instrumental responding. J Neurosci 27(51):13977–13981

    Article  PubMed  CAS  Google Scholar 

  • Courtiere A, Hardouin J, Locatelli V, Turle-Lorenzo N, Amalric M, Vidal F, Hasbroucq T (2005) Selective effects of partial striatal 6-OHDA lesions on information processing in the rat. Eur J NeuroSci 21(7):1973–1983

    Article  PubMed  Google Scholar 

  • Cousins MS, Trevitt J, Atherton A, Salamone JD (1999) Different behavioral functions of dopamine in the nucleus accumbens and ventrolateral striatum: a microdialysis and behavioral investigation. Neuroscience 91(3):925–934

    Article  PubMed  CAS  Google Scholar 

  • Crespi LP (1942) Quantitative variation of incentive and performance in the white rat. Am J Psychol 55:467–517

    Article  Google Scholar 

  • Cromwell HC, Schultz W (2003) Effects of expectations for different reward magnitudes on neuronal activity in primate striatum. J Neurophysiol 89(5):2823–2838

    Article  PubMed  Google Scholar 

  • Dalley JW, Fryer TD, Brichard L, Robinson ES, Theobald DE, Laane K, Pena Y, Murphy ER, Shah Y, Probst K, Abakumova I, Aigbirhio FI, Richards HK, Hong Y, Baron JC, Everitt BJ, Robbins TW (2007) Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science 315(5816):1267–1270

    Article  PubMed  CAS  Google Scholar 

  • Denk F, Walton ME, Jennings KA, Sharp T, Rushworth MF, Bannerman DM (2005) Differential involvement of serotonin and dopamine systems in cost-benefit decisions about delay or effort. Psychopharmacology (Berl) 179(3):587–596

    Article  CAS  Google Scholar 

  • Estes WK (1943) Discriminative conditioning. I. A discriminative property of conditioned anticipation. J Exp Psychol 32:150–155

    Article  Google Scholar 

  • Faure A, Haberland U, Conde F, El Massioui N (2005) Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation. J Neurosci 25(11):2771–2780

    Article  PubMed  CAS  Google Scholar 

  • Featherstone RE, McDonald RJ (2004) Dorsal striatum and stimulus-response learning: lesions of the dorsolateral, but not dorsomedial, striatum impair acquisition of a simple discrimination task. Behav Brain Res 150(1–2):15–23

    Article  PubMed  CAS  Google Scholar 

  • Giertler C, Bohn I, Hauber W (2005) Involvement of NMDA and AMPA/KA receptors in the nucleus accumbens core in instrumental learning guided by reward-predictive cues. Eur J NeuroSci 21(6):1689–1702

    Article  PubMed  Google Scholar 

  • Gold JI (2003) Linking reward expectation to behavior in the basal ganglia. Trends Neurosci 26(1):12–14

    Article  PubMed  CAS  Google Scholar 

  • Hassani OK, Cromwell HC, Schultz W (2001) Influence of expectation of different rewards on behavior-related neuronal activity in the striatum. J Neurophysiol 85(6):2477–2489

    PubMed  CAS  Google Scholar 

  • Hikosaka O, Nakamura K, Nakahara H (2006) Basal ganglia orient eyes to reward. J Neurophysiol 95(2):567–584

    Article  PubMed  Google Scholar 

  • Jog MS, Kubota Y, Connolly CI, Hillegaart V, Graybiel AM (1999) Building neural representations of habits. Science 286(5445):1745–1749

    Article  PubMed  CAS  Google Scholar 

  • Kawagoe R, Takikawa Y, Hikosaka O (1998) Expectation of reward modulates cognitive signals in the basal ganglia. Nature Neurosci 1(5):411–416

    Article  PubMed  CAS  Google Scholar 

  • Lovibond PF (1983) Facilitation of instrumental behavior by a Pavlovian appetitive conditioned stimulus. J Exp Psychol Anim Behav Process 9(3):225–247

    Article  PubMed  CAS  Google Scholar 

  • Martin-Iverson MT, Wilkie D, Fibiger HC (1987) Effects of haloperidol and d-amphetamine on perceived quantity of food and tones. Psychopharmacology (Berl) 93(3):374–381

    Article  CAS  Google Scholar 

  • McGeorge AJ, Faull RL (1989) The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29(3):503–537

    Article  PubMed  CAS  Google Scholar 

  • McSweeney FK (1975) Matching and contrast on several concurrent treadle-press schedules. J Exp Anal Behav 23(2):193–198

    Article  PubMed  Google Scholar 

  • Nakamura K, Hikosaka O (2006) Role of dopamine in the primate caudate nucleus in reward modulation of saccades. J Neurosci 26(20):5360–5369

    Article  PubMed  CAS  Google Scholar 

  • O’Brien CP, Childress AR, Ehrman R, Robbins SJ (1998) Conditioning factors in drug abuse can they explain compulsion? J Psychopharmacol 12(1):15–22

    Article  PubMed  CAS  Google Scholar 

  • O’Neill M, Brown VJ (2007) The effect of striatal dopamine depletion and the adenosine A2A antagonist KW-6002 on reversal learning in rats. Neurobiol Learn Mem 88(1):75–81

    Article  PubMed  CAS  Google Scholar 

  • Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates. Academic, New York

    Google Scholar 

  • Ragozzino ME (2007) The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. Ann N Y Acad Sci 1121:355–375

    Article  PubMed  Google Scholar 

  • Ragozzino ME, Ragozzino KE, Mizumori SJ, Kesner RP (2002) Role of the dorsomedial striatum in behavioral flexibility for response and visual cue discrimination learning. Behav Neurosci 116(1):105–115

    Article  PubMed  Google Scholar 

  • 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(2):221–229

    Article  PubMed  CAS  Google Scholar 

  • Samejima K, Ueda Y, Doya K, Kimura M (2005) Representation of action-specific reward values in the striatum. Science 310(5752):1337–1340

    Article  PubMed  CAS  Google Scholar 

  • Schoenbaum G, Chiba AA, Gallagher M (2000) Changes in functional connectivity in orbitofrontal cortex and basolateral amygdala during learning and reversal training. J Neurosci 20(13):5179–5189

    PubMed  CAS  Google Scholar 

  • Schultz W (2007) Behavioral dopamine signals. Trends Neurosci 30(5):203–210

    Article  PubMed  CAS  Google Scholar 

  • Tobler PN, Fiorillo CD et al (2005) Adaptive coding of reward value by dopamine neurons. Science 307(5715):1642–1645

    Article  PubMed  CAS  Google Scholar 

  • Tremblay L, Schultz W (1999) Relative reward preference in primate orbitofrontal cortex. Nature 398(6729):704–708

    Article  PubMed  CAS  Google Scholar 

  • Tremblay L, Hollerman JR, Schultz W (1998) Modifications of reward expectation-related neuronal activity during learning in primate striatum. J Neurophysiol 80(2):964–977

    PubMed  CAS  Google Scholar 

  • Volkow ND, Wang GJ, Telang F, Fowler JS, Logan J, Childress AR, Jayne M, Ma Y, Wong C (2006) Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J Neurosci 26(24):6583–6588

    Article  PubMed  CAS  Google Scholar 

  • Winkler C, Kirik D, Bjorklund A, Cenci MA (2002) L-DOPA-induced dyskinesia in the intrastriatal 6-hydroxydopamine model of Parkinson’s disease: relation to motor and cellular parameters of nigrostriatal function. Neurobiol Dis 10(2):165–186

    Article  PubMed  Google Scholar 

  • Winstanley CA, Theobald DE, Cardinal RN, Robbins TW (2004) Contrasting roles of basolateral amygdala and orbitofrontal cortex in impulsive choice. J Neurosci 24(20):4718–4722

    Article  PubMed  CAS  Google Scholar 

  • Winters BD, Robbins TW, Everitt BJ (2004) Selective cholinergic denervation of the cingulate cortex impairs the acquisition and performance of a conditional visual discrimination in rats. Eur J NeuroSci 19(2):490–496

    Article  PubMed  Google Scholar 

  • Yin HH, Knowlton BJ (2004) Contributions of striatal subregions to place and response learning. Learn Mem 11(4):459–463

    Article  PubMed  Google Scholar 

  • Yin HH, Knowlton BJ (2006) The role of the basal ganglia in habit formation. Nat Rev Neurosci 7(6):464–476

    Article  PubMed  CAS  Google Scholar 

  • Yin HH, Knowlton BJ, Balleine BW (2005a) Blockade of NMDA receptors in the dorsomedial striatum prevents action-outcome learning in instrumental conditioning. Eur J NeuroSci 22(2):505–512

    Article  PubMed  Google Scholar 

  • Yin HH, Ostlund SB, Knowlton BJ, Balleine BW (2005b) The role of the dorsomedial striatum in instrumental conditioning. Eur J NeuroSci 22(2):513–523

    Article  PubMed  Google Scholar 

  • Yuan H, Sarre S, Ebinger G, Michotte Y (2005) Histological, behavioural and neurochemical evaluation of medial forebrain bundle and striatal 6-OHDA lesions as rat models of Parkinson’s disease. J Neurosci Methods 144(1):35–45

    Article  PubMed  Google Scholar 

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Acknowledgments

This research was supported by a grant of the DFG (Ha2340/8–1) and the Friedrich-Naumann Stiftung. The authors wish to thank J. Heide for assistance in experiment 3.

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Correspondence to Wolfgang Hauber.

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Calaminus, C., Hauber, W. Modulation of Behavior by Expected Reward Magnitude Depends on Dopamine in the Dorsomedial Striatum. Neurotox Res 15, 97–110 (2009). https://doi.org/10.1007/s12640-009-9009-1

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  • DOI: https://doi.org/10.1007/s12640-009-9009-1

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