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Roles of D1-like dopamine receptors in the nucleus accumbens and dorsolateral striatum in conditioned avoidance responses

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Abstract

Rationale

Aversively motivated learning is more poorly understood than appetitively motivated learning in many aspects, including the role of dopamine receptors in different regions of the striatum.

Objectives

The present study investigated the roles of the D1-like DA receptors in the nucleus accumbens (NAc) and dorsolateral striatum (DLS) on learning and performance of conditioned avoidance responses (CARs).

Methods

Adult male Wistar rats received intraperitoneal (i.p.), intra-NAc, or intra-DLS injections of the D1 dopamine receptor agonist SKF 81297 or the D1 receptor antagonist SCH 23390 20 min before or immediately after a training session in the CAR task two-way active avoidance, carried out 24 h before a test session.

Results

Pre-training administration of SCH 23390, but not SKF 81297, caused a significant decrease in the number of CARs in the test, but not in the training session, when injected into the DLS, or in either session when injected into the NAc. It also caused a significant increase in the number of escape failures in the training session when injected into the NAc. Systemic administration caused a combination of these effects. Post-training administrations of these drugs caused no significant effect.

Conclusions

The results suggest that the D1-like receptors in the NAc and DLS play important, though different, roles in learning and performance of CAR.

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References

  • Aguilar MA, Mari-Sanmillan MI, Morant-Deusa JJ, Minarro J (2000) Different inhibition of conditioned avoidance response by clozapine and DA D-1 and D-2 antagonists in male mice. Behav Neurosci 114:389–400

    Article  PubMed  CAS  Google Scholar 

  • Alexander GE, Crutcher MD, Delong MR (1990) Basal ganglia–thalamocortical circuits — parallel substrates for motor, oculomotor, prefrontal and limbic functions. Prog Brain Res 85:119–146

    Article  PubMed  CAS  Google Scholar 

  • Balleine BW, O’Doherty JP (2010) Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 35:48–69

    Article  PubMed  Google Scholar 

  • Beninger RJ, Rolfe NG (1995) Dopamine D1-like receptor agonists impair responding for conditioned reward in rats. Behav Pharmacol 6:785–793

    Article  PubMed  CAS  Google Scholar 

  • Beninger RJ, Mason ST, Phillips AG, Fibiger HC (1980) The use of conditioned suppression to evaluate the nature of neuroleptic-induced avoidance deficits. J Pharmacol Exp Ther 213:623–627

    PubMed  CAS  Google Scholar 

  • Berridge KC (2007) The debate over dopamine’s role in reward: the case for incentive salience. Psychopharmacology 131:391–431

    Article  Google Scholar 

  • Brischoux F, Chakraborty S, Brierley DI, Ungless MA (2009) Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc Natl Acad Sci U S A 106:4893–4899

    Article  Google Scholar 

  • Carlezon WA, Thomas MJ (2009) Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 56:122–132

    Article  PubMed  CAS  Google Scholar 

  • Da Cunha C, Gevaerd MS, Vital M, Miyoshi E, Andreatini R, Silveira R, Takahashi RN, Canteras NS (2001) Memory disruption in rats with nigral lesions induced by MPTP: a model for early Parkinson’s disease amnesia. Behav Brain Res 124:9–18

    Article  PubMed  Google Scholar 

  • Da Cunha C, Wietzikoski EC, Dombrowski P, Santos LM, Bortolanza M, Boschen SL, Miyoshi E (2009) Learning processing in the basal ganglia: a mosaic of broken mirrors. Behav Brain Res 199:156–169

    Google Scholar 

  • Di Chiara G (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 137:75–114

    Article  PubMed  Google Scholar 

  • Ferreira JGP, Del-Fava F, Hasue RH, Shammah-Lagnado SJ (2008) Organization of ventral tegmental area projections to the ventral tegmental area–nigral complex in the rat. Neuroscience 153:196–213

    Article  PubMed  CAS  Google Scholar 

  • Floresco SB, Phillips AG (1999) Dopamine and hippocampal input to the nucleus accumbens play an essential role in the search for food in an unpredictable environment. Psychobiology 27:277–286

    CAS  Google Scholar 

  • Frank MJ, Seeberger LC, O’Reilly RC (2004) By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science 306:1940–1943

    Article  PubMed  CAS  Google Scholar 

  • Gal G, Schiller D, Weiner I (2005) Latent inhibition is disrupted by nucleus accumbens shell lesion but is abnormally persistent following entire nucleus accumbens lesion: the neural site controlling the expression and disruption of the stimulus preexposure effect. Behav Brain Res 162:246–255

    Article  PubMed  Google Scholar 

  • Gevaerd MS, Miyoshi E, Silveira R, Canteras NS, Takahashi RN, Da Cunha C (2001a) l-dopa restores striatal dopamine level but fails to reverse MPTP-induced memory deficits in rats. Int J Neuropsychopharmacol 4:361–370

    Article  PubMed  CAS  Google Scholar 

  • Gevaerd MS, Takahashi RN, Silveira R, Da Cunha C (2001b) Caffeine reverses the memory disruption induced by intra-nigral MPTP-injection in rats. Brain Res Bull 55:101–106

    Article  PubMed  CAS  Google Scholar 

  • Goto Y, Grace AA (2008) Limbic and cortical information processing in the nucleus accumbens. Trends Neurosci 31:552–558

    Article  PubMed  CAS  Google Scholar 

  • Hernandez-Lopez S, Bargas J, Surmeier DJ, Reyes A, Galarraga E (1987) D1 receptor activation enhances evoked discharge in neostriatal medium spiny neurons by modulating an l-type Ca2+ conductance. J Neurosci Methods 17:3334–3342

    Google Scholar 

  • Hikida T, Kimura K, Wada N, Funabiki K, Nakanishi S (2010) Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior. Neuron 66:896–907

    Article  PubMed  CAS  Google Scholar 

  • Horvitz JC (2000) Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96:651–656

    Article  PubMed  CAS  Google Scholar 

  • Iorio LC, Cohen M, Coffin VL (1991) Anticholinergic drugs potentiate dopamine D1 but not D2 antagonists on a conditioned avoidance task in rats. J Pharmacol Exp Ther 258:118–123

    PubMed  CAS  Google Scholar 

  • Izquierdo LA, Barros DM, da Costa JC, Furini C, Zinn C, Carnmarota M, Bevilaqua LR, Izquierdo I (2007) A link between role of two prefrontal areas in immediate memory and in long-term memory consolidation. Neurobiol Learn Mem 88:160–166

    Article  PubMed  Google Scholar 

  • LaLumiere RT, Nguyen LT, McGaugh JL (2004) Post-training intrabasolateral amygdala infusions of dopamine modulate consolidation of inhibitory avoidance memory: involvement of noradrenergic and cholinergic systems. Eur J Neurosci 20:2804–2810

    Article  PubMed  Google Scholar 

  • Lapointe NP, Guertin PA (2008) Synergistic effects of D-1/5 and 5-HT1a/7 receptor agonists on locomotor movement induction in complete spinal cord-transected mice. J Neurophysiol 100:160–168

    Article  PubMed  CAS  Google Scholar 

  • Lorens SA, Sorensen JP, Harvey JA (1970) Lesions in nuclei accumbens septi of rat — behavioral and neurochemical effects. J Comp Physiol Psychol 73:284

    Article  PubMed  CAS  Google Scholar 

  • Lovinger DM (2010) Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 58:951–961

    Article  PubMed  CAS  Google Scholar 

  • Maia TV (2010) Two-factor theory, the actor–critic model, and conditioned avoidance. Learn Behav 38:50–67

    Article  PubMed  Google Scholar 

  • Matamales M, Bertran-Gonzalez J, Salomon L, Degos B, Deniau JM, Valjent E, Herve D, Girault JA (2009) Striatal medium-sized spiny neurons: identification by nuclear staining and study of neuronal subpopulations in bac transgenic mice. PLoS One 4:e4770

    Article  PubMed  Google Scholar 

  • Matsumoto M, Hikosaka O (2009) Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459:838–842

    Article  Google Scholar 

  • McGaugh JL, Roozendaal B (2009) Drug enhancement of memory consolidation: historical perspective and neurobiological implications. Psychopharmacology 202:3–14

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Morris G, Schmidt R, Bergman H (2010) Striatal action-learning based on dopamine concentration. Exp Brain Res 200:307–317

    Article  PubMed  Google Scholar 

  • Moutoussis M, Bentall RP, Williams J, Dayan P (2008) A temporal difference account of avoidance learning. Netw Comput Neural Syst 19:137–160

    Article  Google Scholar 

  • Nauta WJH, Smith GP, Faull RLM, Domesick VB (1978) Efferent connections and nigral afferents of nucleus accumbens septi in rat. Neuroscience 3:385–401

    Article  PubMed  CAS  Google Scholar 

  • Nicola SM (2007) The nucleus accumbens as part of a basal ganglia action selection circuit. Psychopharmacology 191:521–550

    Article  PubMed  CAS  Google Scholar 

  • Nicola SM, Surmeier DT, Malenka RC (2000) Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23:185–215

    Article  PubMed  CAS  Google Scholar 

  • Ogren SO, Archer T (1994) Effects of typical and atypical antipsychotic-drugs on 2-way active-avoidance — relationship to DA receptor blocking profile. Psychopharmacology 114:383–391

    Article  PubMed  CAS  Google Scholar 

  • Oliveira AR, Reimer AE, Brandao ML (2009) Role of dopamine receptors in the ventral tegmental area in conditioned fear. Behav Brain Res 199:271–277

    Article  PubMed  Google Scholar 

  • Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates. Academic Press, San Diego, EUA

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

    Article  PubMed  Google Scholar 

  • Redgrave P, Gurney K, Reynolds J (2008) What is reinforced by phasic dopamine signals? Brain Res Rev 58:322–339

    Article  PubMed  CAS  Google Scholar 

  • Reis FLV, Masson S, de Oliveira AR, Brandao ML (2004) Dopaminergic mechanisms in the conditioned and unconditioned fear as assessed by the two-way avoidance and light switch-off tests. Pharmacol Biochem Behav 79:359–365

    Article  PubMed  CAS  Google Scholar 

  • Rossato JI, Bevilaqua LRM, Izquierdo I, Medina JH, Cammarota M (2009) Dopamine controls persistence of long-term memory storage. Science 325:1017–1020

    Article  PubMed  CAS  Google Scholar 

  • Schmidt HD, Pierce RC (2006) Cooperative activation of D1-like and D2-like dopamine receptors in the nucleus accumbens shell is required for the reinstatement of cocaine-seeking behavior in the rat. Neuroscience 142:451–461

    Article  PubMed  CAS  Google Scholar 

  • Schultz W (2010) Dopamine signals for reward value and risk: basic and recent data. Behav Brain Funct 6:9

    Article  Google Scholar 

  • Sesack SR, Grace AA (2010) Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35:27–47

    Article  PubMed  Google Scholar 

  • Shen WX, Flajolet M, Greengard P, Surmeier DJ (2008) Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321:848–851

    Article  PubMed  CAS  Google Scholar 

  • Stuchlik A, Vales K (2006) Effect of dopamine D1 receptor antagonist SCH23390 and D1 agonist a77636 on active allothetic place avoidance, a spatial cognition task. Behav Brain Res 172:250–255

    Article  PubMed  CAS  Google Scholar 

  • Surmeier DJ, Ding J, Day M, Wang ZF, Shen WX (2007) D1 and D2 dopamine-receptor modulation of striatal glutamatergic signalling in striatal medium spiny neurons. Trends Neurosci 30:228–235

    Article  PubMed  CAS  Google Scholar 

  • Torras-Garcia M, Costa-Miserachs D, Morgado-Bernal I, Portell-Cortes I (2003) Improvement of shuttle-box performance by anterodorsal medial septal lesions in rats. Behav Brain Res 141:147–158

    Article  PubMed  Google Scholar 

  • Voorn P, Vanderschuren L, Groenewegen HJ, Robbins TW, Pennartz CMA (2004) Putting a spin on the dorsal–ventral divide of the striatum. Trends Neurosci 27:468–474

    Article  PubMed  CAS  Google Scholar 

  • Wadenberg ML (1992) Antagonism by 8-OH-DPAT, but not ritanserin, of catalepsy induced by SCH-23390 in the rat. J Neural Transm Gen Sect 89:49–59

    Article  PubMed  CAS  Google Scholar 

  • West AR, Grace AA (2002) Opposite influences of endogenous dopamine D-1 and D-2 receptor activation on activity states and electrophysiological properties of striatal neurons: studies combining in vivo intracellular recordings and reverse microdialysis. J Neurosci 22:294–304

    PubMed  CAS  Google Scholar 

  • Wickens JR, Horvitz JC, Costa RM, Killcross S (2007) Dopaminergic mechanisms in actions and habits. J Neurosci 27:8181–8183

    Article  PubMed  CAS  Google Scholar 

  • Wiecki TV, Frank MJ (2010) Neurocomputational models of motor and cognitive deficits in Parkinson’s disease. Recent advances in Parkinson’s disease: basic research. Prog Brain Res 183:275–297

    Article  PubMed  CAS  Google Scholar 

  • Williams GV, Castner SA (2006) Under the curve: critical issues for elucidating D1 receptor function in working memory. Neuroscience 139:263–276

    Article  PubMed  CAS  Google Scholar 

  • Wise RA (2008) Dopamine and reward: the anhedonia hypothesis 30 years on. Neurotox Res 14:69–83

    Article  Google Scholar 

  • Woodruff ML, Fish BS, Alderman AO (1977) Epileptiform lesions in rat hippocampus and acquisition of 2-way avoidance. Physiol Behav 19:401–410

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yin HH, Knowlton BJ, Balleine BW (2006) Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning. Behav Brain Res 166:189–196

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Departamento de Farmacologia, Laboratório de Fisiologia e Farmacologia do Sistema Nervoso Centra, C.P. 19.031, 81.531-980 UFPR, Curitiba, PR, Brazil

    Evellyn Claudia Wietzikoski, Suelen Lúcio Boschen, Edmar Miyoshi, Mariza Bortolanza, Lucélia Mendes dos Santos & Claudio Da Cunha

  2. Departamento de Ciências Farmacêuticas, UEPG, Ponta Grossa, Brazil

    Edmar Miyoshi

  3. Department of Cognitive, Linguistic and Psychological Sciences, Department of Psychiatry and Human Behavior, Brown Institute for Brain Science, Brown University, 190 Thayer St, Providence, RI, 02912-1978, USA

    Michael Frank

  4. Instituto de Neurociencias e Comportamento – IneC, Ribeirão Preto, SP, Brazil

    Marcus Lira Brandão

  5. Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, 161 Cathedral Street, Glasgow, G4 0RE, Scotland, UK

    Philip Winn

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  1. Evellyn Claudia Wietzikoski
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  2. Suelen Lúcio Boschen
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  4. Mariza Bortolanza
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  5. Lucélia Mendes dos Santos
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  8. Philip Winn
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  9. Claudio Da Cunha
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Correspondence to Claudio Da Cunha.

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Wietzikoski, E.C., Boschen, S.L., Miyoshi, E. et al. Roles of D1-like dopamine receptors in the nucleus accumbens and dorsolateral striatum in conditioned avoidance responses. Psychopharmacology 219, 159–169 (2012). https://doi.org/10.1007/s00213-011-2384-3

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  • DOI: https://doi.org/10.1007/s00213-011-2384-3

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