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Activation of cannabinoid system in anterior cingulate cortex and orbitofrontal cortex modulates cost-benefit decision making

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Abstract

Despite the evidence for altered decision making in cannabis abusers, the role of the cannabinoid system in decision-making circuits has not been studied. Here, we examined the effects of cannabinoid modulation during cost-benefit decision making in the anterior cingulate cortex (ACC) and orbitofrontal cortex (OFC), key brain areas involved in decision making. We trained different groups of rats in a delay-based and an effort-based form of cost-benefit T-maze decision-making task. During test days, the rats received local injections of either vehicle or ACEA, a cannabinoid type-1 receptor (CB1R) agonist in the ACC or OFC. We measured spontaneous locomotor activity following the same treatments and characterized CB1Rs localization on different neuronal populations within these regions using immunohistochemistry. We showed that CB1R activation in the ACC impaired decision making such that rats were less willing to invest physical effort to gain high reward. Similarly, CB1R activation in the OFC induced impulsive pattern of choice such that rats preferred small immediate rewards to large delayed rewards. Control tasks ensured that the effects were specific for differential cost-benefit tasks. Furthermore, we characterized widespread colocalizations of CB1Rs on GABAergic axonal ends but few colocalizations on glutamatergic, dopaminergic, and serotonergic neuronal ends. These results provide first direct evidence that the cannabinoid system plays a critical role in regulating cost-benefit decision making in the ACC and OFC and implicate cannabinoid modulation of synaptic ends of predominantly interneurons and to a lesser degree other neuronal populations in these two frontal regions.

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Acknowledgments

This work was supported by The European Young Investigator Award (EURYI) grant PE0033-117106. Confocal microscopy analysis was performed at the “Servicio de Microscopia Analítica y de Alta Resolución en Biomedicina” (High Resolution Analytical Microscopy Services for Biomedicine) at the University of the Basque Country (UPV/EHU). The authors would like to thank Z. Fattahi and M. Moradi for their assistance in the experiments and C. Lamy and J.V. Lafuente for helpful comments on the earlier versions of this manuscript.

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The authors declare no conflicts of interest.

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Authors and Affiliations

  1. Visual Cognition Laboratory, Department of Medicine, University of Fribourg, Chemin du Musee 5, CH 1700, Fribourg, Switzerland

    Abbas Khani & Gregor Rainer

  2. Center for Cognition, University of Fribourg, Chemin du Musee 5, CH 1700, Fribourg, Switzerland

    Abbas Khani & Gregor Rainer

  3. Neuroscience Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Mojtaba Kermani, Soghra Hesam & Abbas Haghparast

  4. Department of Medicine, University of Fribourg, Fribourg, Switzerland

    Enrike G. Argandoña

  5. Laboratory of Experimental Neuroscience (LaNCE), University of the Basque Country (UPV/EHU), Leioa, Spain

    Enrike G. Argandoña

  6. Visual & Cognitive Neuroscience Laboratory, Dept of Optometry & Vision Science, University of Melbourne, Parkville, Australia

    Mojtaba Kermani

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  1. Abbas Khani
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  2. Mojtaba Kermani
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Correspondence to Gregor Rainer.

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Khani, A., Kermani, M., Hesam, S. et al. Activation of cannabinoid system in anterior cingulate cortex and orbitofrontal cortex modulates cost-benefit decision making. Psychopharmacology 232, 2097–2112 (2015). https://doi.org/10.1007/s00213-014-3841-6

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