Prefronto-subcortical imbalance characterizes poor decision-making: neurochemical and neural functional evidences in rats
Brain Struct Funct. 2014-08-19; 220(6): 3485-3496
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Fitoussi A(1)(2), Le Moine C(1)(2), De Deurwaerdère P(1)(3), Laqui M(1)(2), Rivalan M(1)(2)(4), Cador M(1)(2), Dellu-Hagedorn F(5)(6).
(1)University of Bordeaux, INCIA, CNRS UMR 5287, PB. 31, 146 rue Léo Saignat, 33076, Bordeaux Cedex, France.
(2)CNRS, University of Bordeaux, INCIA, UMR 5287, 33000, Bordeaux, France.
(3)CNRS, University of Bordeaux, IMN, UMR 5293, 33000, Bordeaux, France.
(4)Institut of Cognitive Neurobiology, Humboldt University Berlin, Berlin, Germany.
(5)University of Bordeaux, INCIA, CNRS UMR 5287, PB. 31, 146 rue Léo Saignat, 33076, Bordeaux Cedex, France.
(6)CNRS, University of Bordeaux, INCIA, UMR 5287, 33000, Bordeaux, France. .
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.