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Inter-individual differences in decision-making, flexible and goal-directed behaviors: novel insights within the prefronto-striatal networks

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Abstract

Inflexible behavior is a hallmark of several decision-making-related disorders such as ADHD and addiction. As in humans, a subset of healthy rats makes poor decisions and prefers immediate larger rewards despite suffering large losses in a rat gambling task (RGT). They also display a combination of traits reminiscent of addiction, notably inflexible behavior and perseverative responses. The goal of the present work was twofold: (1) to elucidate if behavioral inflexibility of poor decision-makers could be related to a lower quality of goal-directed behavior (action–outcome associations); (2) to uncover the neural basis of inter-individual differences in goal-directed behavior. We specifically assessed inter-individual differences in decision-making in the RGT, flexibility in the RGT-reversed version and goal-directed behavior in a contingency degradation test, i.e., response adaptation when dissociating reward delivery from the animal’s action. The contributions of the medial prefrontal cortex and the dorsal striatum to action–outcome associations were assessed using Zif268 immunodetection. Inflexible behavior was related to a lower sensitivity to contingency degradation in all poor decision-makers and only in a few good decision-makers. This poorer sensitivity was associated with a lower immunoreactivity in prelimbic and infralimbic cortices and a higher one in the dorsomedial and dorsolateral striatum. These findings suggest that an imbalanced prefronto-striatal activity could underlie inaccurate goal representation in changing environments and may promote maladaptive habit formation among poor decision-makers. These data strengthen our previous work identifying biomarkers of vulnerability to develop psychiatric disorders and demonstrate the relevance of inter-individual differences to model maladaptive behaviors.

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References

  • Balleine BW, Dickinson A (1998) Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 37:407–419

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Balleine BW, Killcross AS, Dickinson A (2003) The effect of lesions of the basolateral amygdala on instrumental conditioning. J Neurosci 23:666–675

    CAS  PubMed  Google Scholar 

  • Bardo MT, Donohew RL, Harrington NG (1996) Psychobiology of novelty seeking and drug seeking behavior. Behav Brain Res 77:23–43

    Article  CAS  PubMed  Google Scholar 

  • Bechara A, Damasio H (2002) Decision-making and addiction (part I): impaired activation of somatic states in substance dependent individuals when pondering decisions with negative future consequences. Neuropsychologia 40:1675–1689

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bechara A, Damasio H, Tranel D, Damasio AR (1997) Deciding advantageously before knowing the advantageous strategy. Science 275:1293–1295

    Article  CAS  PubMed  Google Scholar 

  • Bechara A, Dolan S, Hindes A (2002) Decision-making and addiction (part II): myopia for the future or hypersensitivity to reward? Neuropsychologia 40:1690–1705

    Article  PubMed  Google Scholar 

  • Belin D, Deroche-Gamonet V (2012) Responses to novelty and vulnerability to cocaine addiction: contribution of a multi-symptomatic animal model. Cold Spring Harb Perspect Med 2(11):a011940. doi:10.1101/cshperspect.a011940

    Article  PubMed  PubMed Central  Google Scholar 

  • Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28:309–369

    Article  CAS  PubMed  Google Scholar 

  • Blondeau C, Dellu-Hagedorn F (2007) Dimensional analysis of ADHD subtypes in rats. Biol Psychiatry 61:1340–1350

    Article  PubMed  Google Scholar 

  • Bozon B, Kelly A, Josselyn SA, Silva AJ, Davis S, Laroche S (2003) MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos Trans R Soc Lond B Biol Sci 358:805–814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradfield LA, Hart G, Balleine BW (2013) The role of the anterior, mediodorsal, and parafascicular thalamus in instrumental conditioning. Front Syst Neurosci 7:51

    Article  PubMed  PubMed Central  Google Scholar 

  • Calu DJ, Stalnaker TA, Franz TM, Singh T, Shaham Y, Schoenbaum G (2007) Withdrawal from cocaine self-administration produces long-lasting deficits in orbitofrontal-dependent reversal learning in rats. Learn Mem 14:325–328

    Article  PubMed  PubMed Central  Google Scholar 

  • Clark L, Cools R, Robbins TW (2004) The neuropsychology of ventral prefrontal cortex: decision-making and reversal learning. Brain Cogn 55:41–53

    Article  CAS  PubMed  Google Scholar 

  • Corbit LH, Balleine BW (2003) The role of prelimbic cortex in instrumental conditioning. Behav Brain Res 146:145–157

    Article  PubMed  Google Scholar 

  • Corbit LH, Muir JL, Balleine BW (2003) Lesions of mediodorsal thalamus and anterior thalamic nuclei produce dissociable effects on instrumental conditioning in rats. Eur J Neurosci 18:1286–1294

    Article  PubMed  Google Scholar 

  • Coutureau E, Esclassan F, Di Scala G, Marchand AR (2012) The role of the rat medial prefrontal cortex in adapting to changes in instrumental contingency. PLoS One 7:e33302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dalley JW, Everitt BJ, Robbins TW (2011) Impulsivity, compulsivity, and top-down cognitive control. Neuron 69:680–694

    Article  CAS  PubMed  Google Scholar 

  • de Visser L et al (2011) Rodent versions of the Iowa gambling task: opportunities and challenges for the understanding of decision-making. Front Neurosci 5:109

    PubMed  PubMed Central  Google Scholar 

  • de Wit S, Watson P, Harsay HA, Cohen MX, van de Vijver I, Ridderinkhof KR (2012) Corticostriatal connectivity underlies individual differences in the balance between habitual and goal-directed action control. J Neurosci 32:12066–12075

    Article  PubMed  Google Scholar 

  • Deroche-Gamonet V, Belin D, Piazza PV (2004) Evidence for addiction-like behavior in the rat. Science 305:1014–1017

    Article  CAS  PubMed  Google Scholar 

  • DSM-V (2013) Diagnostic and statistical manual of mental disorders, Fifth edn. American Psychiatric Association, Washington, DC

    Google Scholar 

  • Ernst M et al (2004) Choice selection and reward anticipation: an fMRI study. Neuropsychologia 42:1585–1597

    Article  PubMed  Google Scholar 

  • Evenden J, Ko T (2005) The psychopharmacology of impulsive behaviour in rats VIII: effects of amphetamine, methylphenidate, and other drugs on responding maintained by a fixed consecutive number avoidance schedule. Psychopharmacology 180:294–305

    Article  CAS  PubMed  Google Scholar 

  • Everitt BJ, Robbins TW (2013) From the ventral to the dorsal striatum: devolving views of their roles in drug addiction. Neurosci Biobehav Rev 37:1946–1954

    Article  PubMed  Google Scholar 

  • Fellows LK (2004) The cognitive neurosciences of human decision making: a review and conceptual framework. Behav Cogn Neurosci Rev 3:159–172

    Article  PubMed  Google Scholar 

  • Fitoussi A, Le Moine C, De Deurwaerdere P, Laqui M, Rivalan M, Cador M, Dellu-Hagedorn F (2015) Prefronto-subcortical imbalance characterizes poor decision-making: neurochemical and neural functional evidences in rats. Brain Struct Funct 220:3485–3496

    Article  CAS  PubMed  Google Scholar 

  • Flagel SB, Akil H, Robinson TE (2009) Individual differences in the attribution of incentive salience to reward-related cues: implications for addiction. Neuropharmacology 56(Suppl 1):139–148

    Article  CAS  PubMed  Google Scholar 

  • Floresco SB, Zhang Y, Enomoto T (2009) Neural circuits subserving behavioral flexibility and their relevance to schizophrenia. Behav Brain Res 204:396–409

    Article  PubMed  Google Scholar 

  • Gillan CM, Papmeyer M, Morein-Zamir S, Sahakian BJ, Fineberg NA, Robbins TW, de Wit S (2011) Disruption in the balance between goal-directed behavior and habit learning in obsessive-compulsive disorder. Am J Psychiatry 168:718–726

    Article  PubMed  PubMed Central  Google Scholar 

  • Goudriaan AE, Oosterlaan J, de Beurs E, van den Brink W (2006) Neurocognitive functions in pathological gambling: a comparison with alcohol dependence, Tourette syndrome and normal controls. Addiction 101:534–547

    Article  PubMed  Google Scholar 

  • Griffiths KR, Morris RW, Balleine BW (2014) Translational studies of goal-directed action as a framework for classifying deficits across psychiatric disorders. Front Syst Neurosci 8:101

    Article  PubMed  PubMed Central  Google Scholar 

  • Jentsch JD, Olausson P, De La Garza R, Taylor JR 2nd (2002) Impairments of reversal learning and response perseveration after repeated, intermittent cocaine administrations to monkeys. Neuropsychopharmacology 26:183–190

    Article  CAS  PubMed  Google Scholar 

  • Kabbaj M, Akil H (2001) Individual differences in novelty-seeking behavior in rats: a c-fos study. Neuroscience 106:535–545

    Article  CAS  PubMed  Google Scholar 

  • Killcross S, Coutureau E (2003) Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 13:400–408

    Article  PubMed  Google Scholar 

  • Koolhaas JM, de Boer SF, Buwalda B, van Reenen K (2007) Individual variation in coping with stress: a multidimensional approach of ultimate and proximate mechanisms. Brain Behav Evol 70:218–226

    Article  PubMed  Google Scholar 

  • LaPorte JL, Egan RJ, Hart PC, Bergner CL, Cachat JM, Canavello PR, Kalueff AV (2010) Qui non proficit, deficit: experimental models for ‘integrative’ research of affective disorders. J Affect Disord 121:1–9

    Article  PubMed  Google Scholar 

  • Lee D, Seo H, Jung MW (2012) Neural basis of reinforcement learning and decision making. Annu Rev Neurosci 35:287–308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maroteaux M, Valjent E, Longueville S, Topilko P, Girault JA, Herve D (2014) Role of the plasticity-associated transcription factor zif268 in the early phase of instrumental learning. PLoS One 9:e81868

    Article  PubMed  PubMed Central  Google Scholar 

  • Matzel LD, Kolata S (2010) Selective attention, working memory, and animal intelligence. Neurosci Biobehav Rev 34:23–30

    Article  PubMed  Google Scholar 

  • Millan EZ, Marchant NJ, McNally GP (2011) Extinction of drug seeking. Behav Brain Res 217:454–462

    Article  CAS  PubMed  Google Scholar 

  • Naneix F, Marchand AR, Di Scala G, Pape JR, Coutureau E (2009) A role for medial prefrontal dopaminergic innervation in instrumental conditioning. J Neurosci 29:6599–6606

    Article  CAS  PubMed  Google Scholar 

  • Orgaz C, Estevez A, Matute H (2013) Pathological gamblers are more vulnerable to the illusion of control in a standard associative learning task. Front Psychol 4:306

    Article  PubMed  PubMed Central  Google Scholar 

  • Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, 3rd edn. Academic Press, San Diego

    Google Scholar 

  • Peters J, LaLumiere RT, Kalivas PW (2008) Infralimbic prefrontal cortex is responsible for inhibiting cocaine seeking in extinguished rats. J Neurosci 28:6046–6053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivalan M, Ahmed SH, Dellu-Hagedorn F (2009a) Risk-prone individuals prefer the wrong options on a rat version of the Iowa gambling task. Biol Psychiatry 66:743–749

    Article  PubMed  Google Scholar 

  • Rivalan M, Blondeau C, Dellu-Hagedorn F (2009b) Modeling symptoms of mental disorders using a dimensional approach in the rat. In: Granon S (ed) Endophenotypes of psychiatric and neurodegenerative disorders in rodent models. Transworld Research Network, Kerala

    Google Scholar 

  • Rivalan M, Coutureau E, Fitoussi A, Dellu-Hagedorn F (2011) Inter-individual decision-making differences in the effects of cingulate, orbitofrontal, and prelimbic cortex lesions in a rat gambling task. Front Behav Neurosci 5:22

    Article  PubMed  PubMed Central  Google Scholar 

  • Rivalan M, Valton V, Series P, Marchand AR, Dellu-Hagedorn F (2013) Elucidating poor decision-making in a rat gambling task. PLoS One 8:e82052

    Article  PubMed  PubMed Central  Google Scholar 

  • Robbins TW, Gillan CM, Smith DG, de Wit S, Ersche KD (2012) Neurocognitive endophenotypes of impulsivity and compulsivity: towards dimensional psychiatry. Trends Cogn Sci 16:81–91

    Article  PubMed  Google Scholar 

  • Robinson TE, Yager LM, Cogan ES, Saunders BT (2014) On the motivational properties of reward cues: Individual differences. Neuropharmacology 76(Pt B):450–459

    Article  CAS  PubMed  Google Scholar 

  • Royall DR et al (2002) Executive control function: a review of its promise and challenges for clinical research. A report from the Committee on Research of the American Neuropsychiatric Association. J Neuropsychiatry Clin Neurosci 14:377–405

    Article  PubMed  Google Scholar 

  • Stalnaker TA, Calhoon GG, Ogawa M, Roesch MR, Schoenbaum G (2010) Neural correlates of stimulus–response and response–outcome associations in dorsolateral versus dorsomedial striatum. Front Integr Neurosci 4:12

    Article  PubMed  PubMed Central  Google Scholar 

  • Toplak ME, Sorge GB, Benoit A, West RF, Stanovich KE (2010) Decision-making and cognitive abilities: a review of associations between Iowa gambling task performance, executive functions, and intelligence. Clin Psychol Rev 30:562–581

    Article  PubMed  Google Scholar 

  • Tricomi E, Balleine B, O’Doherty J (2009) A specific role for posterior dorsolateral striatum in human habit learning. Eur J Neurosci 29:2225–2232

    Article  PubMed  PubMed Central  Google Scholar 

  • van den Bos R et al (2013) Cross-species approaches to pathological gambling: a review targeting sex differences, adolescent vulnerability and ecological validity of research tools. Neurosci Biobehav Rev 37:2454–2471

    Article  PubMed  Google Scholar 

  • van den Bos R, Koot S, de Visser L (2014) A rodent version of the Iowa gambling task: 7 years of progress. Front Psychol 5:203

    Article  PubMed  PubMed Central  Google Scholar 

  • Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32–58

    Article  CAS  PubMed  Google Scholar 

  • Williams ZM, Eskandar EN (2006) Selective enhancement of associative learning by microstimulation of the anterior caudate. Nat Neurosci 9:562–568

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  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 

  • 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  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported and funded by the Centre National de la Recherche Scientifique, the University of Bordeaux and the Conseil Régional d’Aquitaine. We thank B. Lorgeoux, S. Lelgouach, A. Fayoux for technical assistance, A. Marchand, S. Parkes and F. Naneix for their helpful comments on the manuscript and editorial assistance.

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Correspondence to Françoise Dellu-Hagedorn.

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Fitoussi, A., Renault, P., Le Moine, C. et al. Inter-individual differences in decision-making, flexible and goal-directed behaviors: novel insights within the prefronto-striatal networks. Brain Struct Funct 223, 897–912 (2018). https://doi.org/10.1007/s00429-017-1530-z

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