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Prefronto-subcortical imbalance characterizes poor decision-making: neurochemical and neural functional evidences in rats

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Abstract

A major challenge of decision-making research in recent years has been to develop models of poor decision-making to identify its neural bases. Toward this goal, we developed a Rat Gambling Task that discerns good and poor decision-makers in a complex and conflicting situation such as the human Iowa Gambling Task. Nothing is known about the role of the monoaminergic modulatory systems in shaping these phenotypes. Moreover, functional and temporal contributions of brain areas during poor compared to good decision-making remains elusive. Good and poor decision-makers were identified in the Rat Gambling Task. We investigated neurobiological correlates of decision-making capacities in (1) dopamine and serotonin turnovers using post-mortem tissue measurements, (2) the neural circuits differentially recruited during decision-making within the prefronto-subcortical network using cellular Fos immunodetection. Imbalance in monoamine metabolism was revealed in poor decision-makers, i.e. a higher infralimbic vs. lower amygdala serotonergic metabolism. Moreover, good decision-making recruited a wide prefronto-subcortical network but once good choices had been made, a disengagement of key prefrontal areas (insular and infralimbic cortices notably) and the amygdala was observed. By contrast, poor decision-making was associated with a strikingly low recruitment of the prefronto-subcortical network, together with sustained amygdala activity. Our results identify two complementary neurobiological substrates characterizing poor decision-makers: imbalanced monoaminergic systems at rest, congruent with their previously identified complex behavioral phenotype, and an aberrant low recruitment of key brain areas for executive functions and affective valence during the process of decision-making. These biomarkers could sustain vulnerability to developing poor decision-making related disorders.

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Acknowledgments

This work was supported and funded by the Centre National de la Recherche Scientifique, the University of Bordeaux, the Conseil Régional d’Aquitaine and by Fondation M. Bleustein-Blanchet pour la Vocation to A. Fitoussi. Philippe De Deurwaerdère acknowledges support from the COST action CM 1103. We thank B. Bontempi and A. Marchand for helpful comments, L. Graham for English editing, S. Lelgouach, A. Fayoux for technical assistance.

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The authors declare no potential conflicts of interest.

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Author notes

  1. Marion Rivalan

    Present address: Institut of Cognitive Neurobiology, Humboldt University Berlin, Berlin, Germany

Authors and Affiliations

  1. University of Bordeaux, INCIA, CNRS UMR 5287, PB. 31, 146 rue Léo Saignat, 33076, Bordeaux Cedex, France

    Aurélie Fitoussi, Catherine Le Moine, Philippe De Deurwaerdère, Matéo Laqui, Marion Rivalan, Martine Cador & Françoise Dellu-Hagedorn

  2. CNRS, University of Bordeaux, INCIA, UMR 5287, 33000, Bordeaux, France

    Aurélie Fitoussi, Catherine Le Moine, Matéo Laqui, Marion Rivalan, Martine Cador & Françoise Dellu-Hagedorn

  3. CNRS, University of Bordeaux, IMN, UMR 5293, 33000, Bordeaux, France

    Philippe De Deurwaerdère

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  1. Aurélie Fitoussi
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Correspondence to Françoise Dellu-Hagedorn.

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Fitoussi, A., Le Moine, C., De Deurwaerdère, P. et al. Prefronto-subcortical imbalance characterizes poor decision-making: neurochemical and neural functional evidences in rats. Brain Struct Funct 220, 3485–3496 (2015). https://doi.org/10.1007/s00429-014-0868-8

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