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Differential effects of environmental enrichment, social-housing, and isolation-rearing on a rat gambling task: Dissociations between impulsive action and risky decision-making

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Abstract

Rationale

Decision-making deficits, measured using the Iowa Gambling Task (IGT), are observed in many psychiatric populations. Additionally, evidence suggests that the environment also influences the development of these same disorders.

Objective

To determine the direct influence of the environment on decision-making by utilizing the rat gambling task (rGT), a risky decision-making test modeled after the IGT.

Methods

Male rats reared in isolation, in pairs, or in an enriched environment were trained on the rGT as adults. During the rGT, animals chose from four different options. The optimal strategy on the rGT and IGT is the same: to favor options associated with smaller immediate rewards and less punishment/loss. Impulsive action is also measured during rGT performance by recording the number of premature responses made, similar to the five-choice serial reaction time task.

Results

Compared to pair-housed rats, isolated and environmentally enriched rats were slower at learning the optimal strategy. However, following training, only isolation-reared rats chose the disadvantageous options more often. Amphetamine altered decision-making on the rGT in socially housed animals, yet isolates were unaffected. Conversely, amphetamine increased premature responding similarly in all groups. This increase was attenuated by prior administration of a dopamine D1 or D2 antagonist; however, the ability of amphetamine to alter decision-making was not blocked by either drug.

Conclusions

Housing environment affects animals’ ability to learn and perform a decision-making task. Additionally, amphetamine’s effect on impulsive action appears to be mediated by the dopaminergic system, whereas its effect on risky decision-making may be mediated by other neurotransmitters.

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References

  • Bardo MT, Hammer RP (1991) Autoradiographic localization of dopamine D1 and D2 receptors in rat nucleus accumbens: resistance to differential rearing conditions. Neuroscience 45:281–290

    Article  PubMed  CAS  Google Scholar 

  • Bardo MT, Bowling SL, Rowlett JK, Manderscheid P, Buxton ST, Dwoskin LP (1995) Environmental enrichment attenuates locomotor sensitization, but not in vitro dopamine release, induced by amphetamine. Pharmacol Biochem Behav 51:397–405

    Article  PubMed  CAS  Google Scholar 

  • Bardo MT, Klebaur JE, Valone JM, Deaton C (2001) Environmental enrichment decreases intravenous self-administration of amphetamine in female and male rats. Psychopharmacology (Berl) 155:278–284

    Article  CAS  Google Scholar 

  • Bechara A, Damasio AR, Damasio H, Anderson SW (1994) Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50:7–15

    Article  PubMed  CAS  Google Scholar 

  • Bechara A, Damasio H, Damasio AR, Lee GP (1999) Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci 19:5473–5481

    PubMed  CAS  Google Scholar 

  • Bechara A, Dolan S, Denburg N, Hindes A, Anderson SW, Nathan PE (2001) Decision-making deficits, linked to a dysfunctional ventromedial prefrontal cortex, revealed in alcohol and stimulant abusers. Neuropsychologia 39:376–389

    Article  PubMed  CAS  Google Scholar 

  • Bickerdike M, Wright I, Marsden C (1993) Social isolation attenuates rat forebrain 5-HT release induced by KCI stimulation and exposure to a novel environment. Behav Pharmacol 4:231–236

    Article  PubMed  CAS  Google Scholar 

  • Bowling SL, Rowlett JK, Bardo MT (1993) The effect of environmental enrichment on amphetamine-stimulated locomotor activity, dopamine synthesis and dopamine release. Neuropharmacology 32:885–893

    Article  PubMed  CAS  Google Scholar 

  • Brenes JC, Rodríguez O, Fornaguera J (2008) Differential effect of environment enrichment and social isolation on depressive-like behavior, spontaneous activity and serotonin and norepinephrine concentration in prefrontal cortex and ventral striatum. Pharmacol Biochem Behav 89:85–93

    Article  PubMed  CAS  Google Scholar 

  • Brown AS (2011) The environment and susceptibility to schizophrenia. Prog Neurobiol 93:23–58

    Article  PubMed  CAS  Google Scholar 

  • Cella M, Dymond S, Cooper A (2010) Impaired flexible decision-making in major depressive disorder. J Affect Disord 124:207–210

    Article  PubMed  Google Scholar 

  • Cole BJ, Robbins TW (1987) Amphetamine impairs the discriminative performance of rats with dorsal noradrenergic bundle lesions on a 5-choice serial reaction time task: new evidence for central dopaminergic-noradrenergic interactions. Psychopharmacology (Berl) 91:458–466

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Crean JP, de Wit H, Richards JB (2000) Reward discounting as a measure of impulsive behavior in a psychiatric outpatient population. Exp Clin Psychopharmacol. 8(2):155–162

    Article  PubMed  CAS  Google Scholar 

  • Dalley JW, Theobald DE, Pereira EAC, Li PMMC, Robbins TW (2002) Specific abnormalities in serotonin release in the prefrontal cortex of isolation-reared rats measured during behavioural performance of a task assessing visuospatial attention and impulsivity. Psychopharmacology (Berl) 164:329–340

    Article  CAS  Google Scholar 

  • Denburg NL, Tranel D, Bechara A (2005) The ability to decide advantageously declines prematurely in some normal older persons. Neuropsychologia 43:1099–1106

    Article  PubMed  CAS  Google Scholar 

  • Djouma E, Card K, Lodge DJ, Lawrence AJ (2006) The CRF1 receptor antagonist, antalarmin, reverses isolation-induced up-regulation of dopamine D2 receptors in the amygdala and nucleus accumbens of fawn-hooded rats. Eur J Neurosci 23:3319–3327

    Article  PubMed  Google Scholar 

  • 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 (Berl) 128:161–170

    Article  CAS  Google Scholar 

  • Fellows LK, Farah MJ (2003) Ventromedial frontal cortex mediates affective shifting in humans: evidence from a reversal learning paradigm. Brain 126:1830–1837

    Article  PubMed  Google Scholar 

  • Fellows LK, Farah MJ (2005) Different underlying impairments in decision-making following ventromedial and dorsolateral frontal lobe damage in humans. Cereb Cortex 15:58–63

    Article  PubMed  Google Scholar 

  • Floor E, Meng L (1996) Amphetamine releases dopamine from synaptic vesicles by dual mechanisms. Neurosci Lett 215:53–56

    Article  PubMed  CAS  Google Scholar 

  • Fone KCF, Porkess MV (2008) Behavioural and neurochemical effects of post-weaning social isolation in rodents—relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 32:1087–1102

    Article  PubMed  CAS  Google Scholar 

  • Garon N, Moore C, Waschbusch DA (2006) Decision making in children with ADHD only, ADHD-anxious/depressed, and control children using a child version of the Iowa Gambling Task. J Atten Disord 9:607–619

    Article  PubMed  Google Scholar 

  • Goudriaan AE, Oosterlaan J, de Beurs E, van den Brink W (2005) Decision making in pathological gambling: a comparison between pathological gamblers, alcohol dependents, persons with Tourette syndrome, and normal controls. Brain Res Cogn Brain Res 23:137–151

    Article  PubMed  Google Scholar 

  • Halperin JM, Healey DM (2011) The influences of environmental enrichment, cognitive enhancement, and physical exercise on brain development: can we alter the developmental trajectory of ADHD? Neurosci Biobehav Rev 35:621–634

    Article  PubMed  Google Scholar 

  • Harrison AA, Everitt BJ, Robbins TW (1997) Central 5-HT depletion enhances impulsive responding without affecting the accuracy of attentional performance: interactions with dopaminergic mechanisms. Psychopharmacology (Berl) 133:329–342

    Article  CAS  Google Scholar 

  • Heidbreder CA, Weiss IC, Domeney AM, Pryce C, Homberg J, Hedou G, Feldon J, Moran MC, Nelson P (2000) Behavioral, neurochemical and endocrinological characterization of the early social isolation syndrome. Neuroscience 100:749–768

    Article  PubMed  CAS  Google Scholar 

  • Hellemans KGC, Nobrega JN, Olmstead MC (2005) Early environmental experience alters baseline and ethanol-induced cognitive impulsivity: relationship to forebrain 5-HT1A receptor binding. Behav Brain Res 159:207–220

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann LC, Schütte SRM, Koch M, Schwabe K (2009) Effect of “enriched environment” during development on adult rat behavior and response to the dopamine receptor agonist apomorphine. Neuroscience 158:1589–1598

    Article  PubMed  CAS  Google Scholar 

  • Jones GH, Marsden CA, Robbins TW (1991) Behavioural rigidity and rule-learning deficits following isolation-rearing in the rat: neurochemical correlates. Behav Brain Res 43:35–50

    Article  PubMed  CAS  Google Scholar 

  • Jones SR, Gainetdinov RR, Wightman RM, Caron MG (1998) Mechanisms of amphetamine action revealed in mice lacking the dopamine transporter. J Neurosci 18:1979–1986

    PubMed  CAS  Google Scholar 

  • King MV, Seeman P, Marsden CA, Fone KCF (2009) Increased dopamine D2High receptors in rats reared in social isolation. Synapse 63:476–483

    Article  PubMed  CAS  Google Scholar 

  • Krech D, Rosenzweig MR, Bennett EL (1962) Relations between chemistry and problem-solving among rats raised in enriched and impoverished environments. J Comp Physiol Psychol 55:801–807

    Article  PubMed  CAS  Google Scholar 

  • Kuczenski R, Segal D (1989) Concomitant characterization of behavioral and striatal neurotransmitter response to amphetamine using in vivo microdialysis. J Neurosci 9:2051–2065

    PubMed  CAS  Google Scholar 

  • Kuramochi M, Nakamura S (2009) Effects of postnatal isolation rearing and antidepressant treatment on the density of serotonergic and noradrenergic axons and depressive behavior in rats. Neuroscience 163:448–455

    Article  PubMed  CAS  Google Scholar 

  • Laviola G, Hannan AJ, Macrì S, Solinas M, Jaber M (2008) Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol Dis 31:159–168

    Article  PubMed  Google Scholar 

  • Malone DT, Kearn CS, Chongue L, Mackie K, Taylor DA (2008) Effect of social isolation on CB1 and D2 receptor and fatty acid amide hydrolase expression in rats. Neuroscience 152:265–272

    Article  PubMed  CAS  Google Scholar 

  • McDonald J (2009) Handbook of biological statistics. Sparky House, Baltimore

    Google Scholar 

  • Nithianantharajah J, Hannan AJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7:697–709

    Article  PubMed  CAS  Google Scholar 

  • Parada M, Hernandez L, Schwartz D, Hoebel BG (1988) Hypothalamic infusion of amphetamine increases serotonin, dopamine and norepinephrine. Physiol Behav 44:607–610

    Article  PubMed  CAS  Google Scholar 

  • Pattij T, Janssen MCW, Vanderschuren LJMJ, Schoffelmeer ANM, van Gaalen MM (2007) Involvement of dopamine D1 and D2 receptors in the nucleus accumbens core and shell in inhibitory response control. Psychopharmacology (Berl) 191:587–598

    Article  CAS  Google Scholar 

  • Perry JL, Stairs DJ, Bardo MT (2008) Impulsive choice and environmental enrichment: effects of d-amphetamine and methylphenidate. Behav Brain Res 193:48–54

    Article  PubMed  CAS  Google Scholar 

  • Robbins TW (2002) The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berl) 163:362–380

    Article  CAS  Google Scholar 

  • Robinson ES, Eagle DM, Economidou D, Theobald DE, Mar AC, Murphy ER, Robbins TW, Dalley JW (2009) Behavioural characterisation of high impulsivity on the 5-choice serial reaction time task: specific deficits in ‘waiting’ versus 'stopping'. Behav Brain Res 196(2):310–316

    Article  PubMed  CAS  Google Scholar 

  • Robinson OJ, Cools R, Sahakian BJ (2012) Tryptophan depletion disinhibits punishment but not reward prediction: implications for resilience. Psychopharmacology (Berl) 219(2):599–605

    Article  CAS  Google Scholar 

  • Rolls ET, Hornak J, Wade D, McGrath J (1994) Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. J Neurol Neurosurg Psychiatr 57:1518–1524

    Article  PubMed  CAS  Google Scholar 

  • Rothman RB, Baumann MH, Dersch CM, Romero DV, Rice KC, Carroll FI, Partilla JS (2001) Amphetamine-type central nervous system stimulants release norepinephrine more potently than they release dopamine and serotonin. Synapse 39:32–41

    Article  PubMed  CAS  Google Scholar 

  • Schrijver NC, Würbel H (2001) Early social deprivation disrupts attentional, but not affective, shifts in rats. Behav Neurosci 115:437–442

    Article  PubMed  CAS  Google Scholar 

  • Shurman B, Horan WP, Nuechterlein KH (2005) Schizophrenia patients demonstrate a distinctive pattern of decision-making impairment on the Iowa Gambling Task. Schizophr Res 72:215–224

    Article  PubMed  Google Scholar 

  • Simon NW, Gilbert RJ, Mayse JD, Bizon JL, Setlow B (2009) Balancing risk and reward: a rat model of risky decision making. Neuropsychopharmacology 34:2208–2217

    Article  PubMed  Google Scholar 

  • Simpson J, Kelly JP (2011) The impact of environmental enrichment in laboratory rats—behavioural and neurochemical aspects. Behav Brain Res 222:246–264

    Article  PubMed  CAS  Google Scholar 

  • Smoski MJ, Lynch TR, Rosenthal MZ, Cheavens JS, Chapman AL, Krishnan RR (2008) Decision-making and risk aversion among depressive adults. J Behav Ther Exp Psychiatry 39:567–576

    Article  PubMed  Google Scholar 

  • Solinas M, Thiriet N, Chauvet C, Jaber M (2010) Prevention and treatment of drug addiction by environmental enrichment. Prog Neurobiol 92:572–592

    Article  PubMed  CAS  Google Scholar 

  • van der Harst JE, Baars A-M, Spruijt BM (2003) Standard housed rats are more sensitive to rewards than enriched housed rats as reflected by their anticipatory behaviour. Behav Brain Res 142:151–156

    Article  PubMed  Google Scholar 

  • Verdejo-Garcia A, Lawrence AJ, Clark L (2008) Impulsivity as a vulnerability marker for substance use disorders: review of findings from high-risk research, problem gamblers and genetic association studies. Neurosci Biobehav Rev 32(4):777–781

    Article  PubMed  Google Scholar 

  • Vitaro F, Arseneault L, Tremblay RE (1999) Impulsivity predicts problem gambling in low SES adolescent males. Addiction 94(4):565–575

    Article  PubMed  CAS  Google Scholar 

  • Welte JW, Barnes GM, Wieczorek WF, Tidwell M-CO, Parker JC (2004) Risk factors for pathological gambling. Addict Behav 29:323–335

    Article  PubMed  Google Scholar 

  • Winstanley CA, Dalley JW, Theobald DE, Robbins TW (2004) Fractionating impulsivity: contrasting effects of central 5-HT depletion on different measures of impulsive behavior. Neuropsychopharmacology. 29(7):1331–1343

    Article  PubMed  CAS  Google Scholar 

  • Zeeb FD, Winstanley CA (2011) Lesions of the basolateral amygdala and orbitofrontal cortex differentially affect acquisition and performance of a rodent gambling task. J Neurosci 31:2197–2204

    Article  PubMed  CAS  Google Scholar 

  • Zeeb FD, Robbins TW, Winstanley CA (2009) Serotonergic and dopaminergic modulation of gambling behavior as assessed using a novel rat gambling task. Neuropsychopharmacology 34:2329–2343

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by an operating grant awarded to CAW from the Canadian Institutes for Health Research (CIHR). CAW also receives salary support through the Michael Smith Foundation for Health Research and the CIHR New Investigator Award program. We would like to thank Chris McKinnon for his enthusiasm and invaluable technical assistance.

Conflict of interest

CAW has previously consulted for Theravance on an unrelated matter. No authors have any other conflicts of interest or financial disclosures to make.

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Correspondence to Fiona D. Zeeb or Catharine A. Winstanley.

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Zeeb, F.D., Wong, A.C. & Winstanley, C.A. Differential effects of environmental enrichment, social-housing, and isolation-rearing on a rat gambling task: Dissociations between impulsive action and risky decision-making. Psychopharmacology 225, 381–395 (2013). https://doi.org/10.1007/s00213-012-2822-x

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