A specific prelimbic-nucleus accumbens pathway controls resilience versus vulnerability to food addiction.
Animals
Disease Models, Animal
Feeding Behavior
/ physiology
Food Addiction
/ genetics
Gene Expression Profiling
Gene Expression Regulation
Mice, Knockout
Neural Pathways
/ physiology
Nucleus Accumbens
/ physiology
Prefrontal Cortex
/ physiology
Receptor, Cannabinoid, CB1
/ genetics
Receptors, Dopamine D2
/ genetics
Synaptic Transmission
Up-Regulation
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
07 02 2020
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
782Références
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