A specific prelimbic-nucleus accumbens pathway controls resilience versus vulnerability to food addiction.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
07 02 2020
Historique:
received: 12 06 2019
accepted: 19 12 2019
entrez: 9 2 2020
pubmed: 9 2 2020
medline: 19 5 2020
Statut: epublish

Résumé

Food addiction is linked to obesity and eating disorders and is characterized by a loss of behavioral control and compulsive food intake. Here, using a food addiction mouse model, we report that the lack of cannabinoid type-1 receptor in dorsal telencephalic glutamatergic neurons prevents the development of food addiction-like behavior, which is associated with enhanced synaptic excitatory transmission in the medial prefrontal cortex (mPFC) and in the nucleus accumbens (NAc). In contrast, chemogenetic inhibition of neuronal activity in the mPFC-NAc pathway induces compulsive food seeking. Transcriptomic analysis and genetic manipulation identified that increased dopamine D2 receptor expression in the mPFC-NAc pathway promotes the addiction-like phenotype. Our study unravels a new neurobiological mechanism underlying resilience and vulnerability to the development of food addiction, which could pave the way towards novel and efficient interventions for this disorder.

Identifiants

pubmed: 32034128
doi: 10.1038/s41467-020-14458-y
pii: 10.1038/s41467-020-14458-y
pmc: PMC7005839
doi:

Substances chimiques

DRD2 protein, mouse 0
Receptor, Cannabinoid, CB1 0
Receptors, Dopamine D2 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

782

Références

Pursey, K. et al. The prevalence of food addiction as assessed by the Yale Food Addiction Scale: a systematic review. Nutrients 6, 4552–4590 (2014).
pubmed: 25338274 pmcid: 4210934 doi: 10.3390/nu6104552
Gordon, E. et al. What Is the evidence for “food addiction?” a systematic review. Nutrients 10, 477 (2018).
pmcid: 5946262 doi: 10.3390/nu10040477
Gearhardt, A. N., Corbin, W. R. & Brownell, K. D. Development of the Yale Food Addiction Scale version 2.0. Psychol. Addict. Behav. 30, 113–121 (2016).
pubmed: 26866783 doi: 10.1037/adb0000136 pmcid: 26866783
Lindgren, E. et al. Food addiction: a common neurobiological mechanism with drug abuse. Front. Biosci. 23, 811–836 (2017).
Mancino, S. et al. Epigenetic and proteomic expression changes promoted by eating addictive-like behavior. Neuropsychopharmacology 10, 2788–800 (2015).
pubmed: 25944409 pmcid: 4864655 doi: 10.1038/npp.2015.129
Koob, G. F. & Volkow, N. D. Neurobiology of addiction: a neurocircuitry analysis. Lancet Psychiatry 3, 760–773 (2016).
pubmed: 6135092 pmcid: 6135092 doi: 10.1016/S2215-0366(16)00104-8
Miller, E. K. & Cohen, J. D. An Integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).
pubmed: 11283309 doi: 10.1146/annurev.neuro.24.1.167 pmcid: 11283309
Blakemore, S. -J. & Robbins, T. W. Decision-making in the adolescent brain. Nat. Neurosci. 15, 1184–1191 (2012).
pubmed: 22929913 doi: 10.1038/nn.3177 pmcid: 22929913
Diamond, A. Executive functions. Annu. Rev. Psychol. 64, 135–168 (2013).
pubmed: 23020641 doi: 10.1146/annurev-psych-113011-143750 pmcid: 23020641
Volkow, N. D., Wang, G. J., Tomasi, D. & Baler, R. D. The addictive dimensionality of obesity. Biol. Psychiatry 73, 811–818 (2013).
Chen, B. T. et al. Rescuing cocaine-induced prefrontal cortex hypoactivity prevents compulsive cocaine seeking. Nature 496, 359–362 (2013).
pubmed: 23552889 doi: 10.1038/nature12024 pmcid: 23552889
Volkow, N. D. et al. Activity in healthy adults. Obesity 17, 60–65 (2010).
doi: 10.1038/oby.2008.469
Riga, D. et al. Optogenetic dissection of medial prefrontal cortex circuitry. Front. Syst. Neurosci. 8, 1–19 (2014).
doi: 10.3389/fnsys.2014.00230
Burns, J. et al. Cannabis addiction and the brain: a review. J. Neuroimmune Pharmacol. 13, 438–452 (2018).
pubmed: 29556883 pmcid: 6223748 doi: 10.1007/s11481-018-9782-9
Hitchcott, P. K., Quinn, J. J. & Taylor, J. R. Bidirectional modulation of goal-directed actions by prefrontal cortical dopamine. Cereb. Cortex 17, 2820–2827 (2007).
pubmed: 17322558 doi: 10.1093/cercor/bhm010 pmcid: 17322558
Monory, K. et al. The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51, 455–466 (2006).
pubmed: 16908411 pmcid: 1769341 doi: 10.1016/j.neuron.2006.07.006
Bellocchio, L. et al. Bimodal control of stimulated food intake by the endocannabinoid system. Nat. Neurosci. 13, 281–283 (2010).
pubmed: 20139974 doi: 10.1038/nn.2494 pmcid: 20139974
Kano, M., Ohno-Shosaku, T., Hashimotodani, Y. & Uchigashima, M. Endocannabinoid-mediated control of synaptic transmission. 309–380 (2009). https://doi.org/10.1152/physrev.00019.2008 .
pubmed: 19126760 doi: 10.1152/physrev.00019.2008 pmcid: 19126760
Goldstein, R. Z. & Volkow, N. D. Dysfunction of the prefrontal cortex in addiction: Neuroimaging findings and clinical implications. Nat. Rev. Neurosci. 12, 652–669 (2011).
pubmed: 22011681 pmcid: 3462342 doi: 10.1038/nrn3119
Marsicano, G. & Kuner, R. in Cannabinoids and the Brain (ed. Kendall, D. A.) 161–201 (Springer, 2008).
Scofield, M. D. et al. The nucleus accumbens: mechanisms of addiction across drug classes reflect the importance of glutamate homeostasis. Pharmacol. Rev. 68, 816–871 (2016).
pubmed: 27363441 pmcid: 4931870 doi: 10.1124/pr.116.012484
Stuber, G. D. et al. Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475, 377–382 (2011).
pubmed: 21716290 pmcid: 3775282 doi: 10.1038/nature10194
Tervo, D. G. R. et al. A designer AAV variant permits efficient retrograde access to projection neurons. Neuron 92, 372–382 (2016).
pubmed: 27720486 pmcid: 5872824 doi: 10.1016/j.neuron.2016.09.021
Kneussel, M. & Wagner, W. Myosin motors at neuronal synapses: drivers of membrane transport and actin dynamics. Nat. Rev. Neurosci. 14, 233–247 (2013).
pubmed: 23481482 doi: 10.1038/nrn3445 pmcid: 23481482
Tan, Z. J., Peng, Y., Song, H. L., Zheng, J. J. & Yu, X. N-cadherin-dependent neuron-neuron interaction is required for the maintenance of activity-induced dendrite growth. Proc. Natl Acad. Sci. U.S.A. 107, 9873–9878 (2010).
pubmed: 20457910 pmcid: 2906874 doi: 10.1073/pnas.1003480107
Urade, Y. & Hayaishi, O. Biochemical, structural, genetic, physiological, and pathophysiological features of lipocalin-type prostaglandin D synthase. Biochim. Biophys. Acta 1482, 259–271 (2000).
pubmed: 11058767 doi: 10.1016/S0167-4838(00)00161-8 pmcid: 11058767
Nestler, E. J. Cellular basis of memory for addiction. Dialogues Clin. Neurosci. 15, 431–443 (2013).
pubmed: 24459410 pmcid: 3898681
Martín-García, E. et al. Differential control of cocaine self-administration by GABAergic and glutamatergic CB1 cannabinoid receptors. Neuropsychopharmacology 1–14 (2015). https://doi.org/10.1038/npp.2015.351 .
pubmed: 26612422 doi: 10.1038/npp.2015.351 pmcid: 26612422
Häring, M., Kaiser, N., Monory, K. & Lutz, B. Circuit specific functions of cannabinoid CB1 receptor in the balance of investigatory drive and exploration. PLoS ONE 6, e26617 (2011).
pubmed: 22069458 pmcid: 3206034 doi: 10.1371/journal.pone.0026617
Lutz, B., Marsicano, G., Maldonado, R. & Hillard, C. J. The endocannabinoid system in guarding against fear, anxiety and stress. Nat. Rev. Neurosci. 16, 705–718 (2015).
pubmed: 26585799 pmcid: 5871913 doi: 10.1038/nrn4036
Steindel, F. et al. Neuron-type specific cannabinoid-mediated G protein signalling in mouse hippocampus. J. Neurochem. 124, 795–807 (2013).
pubmed: 23289830 doi: 10.1111/jnc.12137
Monory, K., Polack, M., Remus, A., Lutz, B. & Korte, M. Cannabinoid CB1 receptor calibrates excitatory synaptic balance in the mouse hippocampus. J. Neurosci. 35, 3842–3850 (2015).
pubmed: 25740514 pmcid: 6605579 doi: 10.1523/JNEUROSCI.3167-14.2015
Wang, W. et al. Regulation of prefrontal excitatory neurotransmission by dopamine in the nucleus accumbens core. J. Physiol. 590, 3743–3769 (2012).
pubmed: 22586226 pmcid: 3476631 doi: 10.1113/jphysiol.2012.235200
Moorman, D. E., James, M. H., McGlinchey, E. M. & Aston-Jones, G. Differential roles of medial prefrontal subregions in the regulation of drug seeking. Brain Res. 1628, 130–146 (2015).
pubmed: 25529632 doi: 10.1016/j.brainres.2014.12.024
Terraneo, A. et al. Transcranial magnetic stimulation of dorsolateral prefrontal cortex reduces cocaine use: a pilot study. Eur. Neuropsychopharmacol. 26, 37–44 (2016).
pubmed: 26655188 doi: 10.1016/j.euroneuro.2015.11.011 pmcid: 26655188
Heidbreder, C. A. & Groenewegen, H. J. The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci. Biobehav. Rev. 27, 555–579 (2003).
pubmed: 14599436 doi: 10.1016/j.neubiorev.2003.09.003
Vertes, R. P. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142, 1–20 (2006).
pubmed: 16887277 doi: 10.1016/j.neuroscience.2006.06.027
McGlinchey, E. M., James, M. H., Mahler, S. V., Pantazis, C. & Aston-Jones, G. Prelimbic to accumbens core pathway is recruited in a dopamine-dependent manner to drive cued reinstatement of cocaine seeking. J. Neurosci. 36, 8700–8711 (2016).
pubmed: 27535915 pmcid: 4987439 doi: 10.1523/JNEUROSCI.1291-15.2016
Schmitzer-Torbert, N. et al. Post-training cocaine administration facilitates habit learning and requires the infralimbic cortex and dorsolateral striatum. Neurobiol. Learn. Mem. 118, 105–112 (2015).
pubmed: 25460040 doi: 10.1016/j.nlm.2014.11.007
Le Merrer, J. et al. Protracted abstinence from distinct drugs of abuse shows regulation of a common gene network. Addict. Biol. 17, 1–12 (2012).
pubmed: 21955143 doi: 10.1111/j.1369-1600.2011.00365.x pmcid: 21955143
Real, J. I., Simões, A. P., Cunha, R. A., Ferreira, S. G. & Rial, D. Adenosine A
pubmed: 29570875 doi: 10.1111/ejn.13912 pmcid: 29570875
Ferre, S. et al. An update on adenosine A2A-dopamine D2 receptor interactions: implications for the function of G protein-coupled receptors. Curr. Pharm. Des. 14, 1468–1474 (2008).
pubmed: 18537670 pmcid: 2424285 doi: 10.2174/138161208784480108
Quintana, A. et al. Lack of GPR88 enhances medium spiny neuron activity and alters motor- and cue-dependent behaviors. Nat. Neurosci. 15, 1547–1555 (2012).
pubmed: 23064379 pmcid: 3483418 doi: 10.1038/nn.3239
Gao, W. J., Krimer, L. S. & Goldman-Rakic, P. S. Presynaptic regulation of recurrent excitation by D1 receptors in prefrontal circuits. Proc. Natl Acad. Sci. U.S.A. 98, 295–300 (2001).
pubmed: 11134520 doi: 10.1073/pnas.98.1.295 pmcid: 11134520
Volkow, N. D. et al. Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse 14, 169–177 (1993).
pubmed: 8101394 doi: 10.1002/syn.890140210 pmcid: 8101394
Blum, K. et al. Increased prevalence of the Taq I A1 allele of the dopamine receptor gene (DRD2) in obesity with comorbid substance use disorder: a preliminary report. Pharmacogenetics 6, 297–305 (1996).
pubmed: 8873216 doi: 10.1097/00008571-199608000-00003 pmcid: 8873216
Cui, Q. et al. Dopamine receptors mediate strategy abandoning via modulation of a specific prelimbic cortex–nucleus accumbens pathway in mice. Proc. Natl Acad. Sci. USA 115, E4890–E4899 (2018).
pubmed: 29735678 doi: 10.1073/pnas.1717106115 pmcid: 29735678
Bock, R. et al. Strengthening the accumbal indirect pathway promotes resilience to compulsive cocaine use. Nat. Neurosci. 16, 632–638 (2013).
pubmed: 23542690 pmcid: 3637872 doi: 10.1038/nn.3369
Martín-García, E. et al. New operant model of reinstatement of food-seeking behavior in mice. Psychopharmacol. (Berl.). 215, 49–70 (2011).
doi: 10.1007/s00213-010-2110-6
Deroche-Gamonet, V., Belin, D. & Piazza, P. V. Evidence for addiction-like behavior in the rat. Science 305, 1014–1017 (2004).
pubmed: 15310906 doi: 10.1126/science.1099020 pmcid: 15310906
Paxinos, G. & Franklin, K. B. J. The Mouse Brain in Stereotaxic Coordinates. (Elsevier, 2001).
Gallo, E. F. et al. Accumbens dopamine D2 receptors increase motivation by decreasing inhibitory transmission to the ventral pallidum. Nat. Commun. 9, 1086 (2018).
pubmed: 29540712 pmcid: 5852096 doi: 10.1038/s41467-018-03272-2
Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511–515 (2010).
pubmed: 20436464 pmcid: 20436464 doi: 10.1038/nbt.1621
Anders, S., Pyl, P. T. & Huber, W. HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015).
pubmed: 25260700 doi: 10.1093/bioinformatics/btu638 pmcid: 25260700
Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
pubmed: 20979621 pmcid: 3218662 doi: 10.1186/gb-2010-11-10-r106

Auteurs

Laura Domingo-Rodriguez (L)

Laboratory of Neuropharmacology-Neurophar, Department of Experimental and Health Sciences, Universitat Pompeu Fabra (UPF), Barcelona, Spain.

Inigo Ruiz de Azua (I)

Institute of Physiological Chemistry, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.
Leibniz Institute for Resilience Research, Mainz, Germany.

Eduardo Dominguez (E)

Centre for genomic regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain.

Eric Senabre (E)

Laboratory of Neuropharmacology-Neurophar, Department of Experimental and Health Sciences, Universitat Pompeu Fabra (UPF), Barcelona, Spain.

Irene Serra (I)

Instituto Cajal, CSIC, Madrid, Spain.

Sami Kummer (S)

Laboratory of Neuropharmacology-Neurophar, Department of Experimental and Health Sciences, Universitat Pompeu Fabra (UPF), Barcelona, Spain.

Mohit Navandar (M)

Faculty of Biology and Center of Computational Sciences, Johannes Gutenberg University, Mainz, Germany.

Sarah Baddenhausen (S)

Institute of Physiological Chemistry, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Clementine Hofmann (C)

Institute of Physiological Chemistry, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.
Focus Program Translational Neuroscience, Johannes Gutenberg University Mainz, Mainz, Germany.

Raul Andero (R)

Department of Psychobiology and Methodology in Health Sciences, Universitat Autònoma de Barcelona (UAB), Bellaterra, Spain.
Instituto de Salud Carlos III, Centro de Investigación Biomédica en Red de Salud Mental, CIBERSAM, Bellaterra, Spain.
Unitat de Neurociència Traslacional, ParcTaulí Hospital Universitari, Institut d'Investigació i Innovació ParcTaulí (I3PT), Institut de Neurociències, UAB, Bellaterra, Spain.

Susanne Gerber (S)

Faculty of Biology and Center of Computational Sciences, Johannes Gutenberg University, Mainz, Germany.

Marta Navarrete (M)

Instituto Cajal, CSIC, Madrid, Spain.

Mara Dierssen (M)

Centre for genomic regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain.
Hospital del Mar Medical Research Institute (IMIM), Barcelona, Spain.

Beat Lutz (B)

Institute of Physiological Chemistry, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.
Leibniz Institute for Resilience Research, Mainz, Germany.

Elena Martín-García (E)

Laboratory of Neuropharmacology-Neurophar, Department of Experimental and Health Sciences, Universitat Pompeu Fabra (UPF), Barcelona, Spain.
Department of Psychobiology and Methodology in Health Sciences, Universitat Autònoma de Barcelona (UAB), Bellaterra, Spain.

Rafael Maldonado (R)

Laboratory of Neuropharmacology-Neurophar, Department of Experimental and Health Sciences, Universitat Pompeu Fabra (UPF), Barcelona, Spain. rafael.maldonado@upf.edu.
Hospital del Mar Medical Research Institute (IMIM), Barcelona, Spain. rafael.maldonado@upf.edu.

Articles similaires

Humans Meals Time Factors Female Adult
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Classifications MeSH