Endocannabinoid Modulation of Nucleus Accumbens Microcircuitry and Terminal Dopamine Release

Overview

Journal Front Synaptic Neurosci

Date 2021 Sep 9

PMID 34497503

Citations 9

Authors

Dan P Covey

Alyssa G Yocky

Affiliations

Soon will be listed here.

Abstract

The nucleus accumbens (NAc) is located in the ventromedial portion of the striatum and is vital to valence-based predictions and motivated action. The neural architecture of the NAc allows for complex interactions between various cell types that filter incoming and outgoing information. Dopamine (DA) input serves a crucial role in modulating NAc function, but the mechanisms that control terminal DA release and its effect on NAc neurons continues to be elucidated. The endocannabinoid (eCB) system has emerged as an important filter of neural circuitry within the NAc that locally shapes terminal DA release through various cell type- and site-specific actions. Here, we will discuss how eCB signaling modulates terminal DA release by shaping the activity patterns of NAc neurons and their afferent inputs. We then discuss recent technological advancements that are capable of dissecting how distinct cell types, their afferent projections, and local neuromodulators influence valence-based actions.

Citing Articles

ABHD6 loss-of-function in mesoaccumbens postsynaptic but not presynaptic neurons prevents diet-induced obesity in male mice.

Lau D, Tobin S, Pribiag H, Nakajima S, Fisette A, Matthys D Nat Commun. 2024; 15(1):10652.

PMID: 39681558 PMC: 11649924. DOI: 10.1038/s41467-024-54819-5.

Exploring the memory: existing activity-dependent tools to tag and manipulate engram cells.

Pang B, Wu X, Chen H, Yan Y, Du Z, Yu Z Front Cell Neurosci. 2024; 17:1279032.

PMID: 38259503 PMC: 10800721. DOI: 10.3389/fncel.2023.1279032.

The endogenous cannabinoid system modulates male sexual behavior expression.

Rodriguez-Manzo G, Canseco-Alba A Front Behav Neurosci. 2023; 17:1198077.

PMID: 37324524 PMC: 10264596. DOI: 10.3389/fnbeh.2023.1198077.

Crosstalk between the endocannabinoid and mid-brain dopaminergic systems: Implication in dopamine dysregulation.

Kibret B, Canseco-Alba A, Onaivi E, Engidawork E Front Behav Neurosci. 2023; 17:1137957.

PMID: 37009000 PMC: 10061032. DOI: 10.3389/fnbeh.2023.1137957.

Motherhood and DREADD manipulation of the nucleus accumbens weaken established pair bonds in female prairie voles.

Forero S, Sailer L, Gircyte A, Madrid J, Sullivan N, Ophir A Horm Behav. 2023; 151:105351.

PMID: 37003159 PMC: 10133177. DOI: 10.1016/j.yhbeh.2023.105351.

References

Reed S, Lafferty C, Mendoza J, Yang A, Davidson T, Grosenick L . Coordinated Reductions in Excitatory Input to the Nucleus Accumbens Underlie Food Consumption. Neuron. 2018; 99(6):1260-1273.e4. DOI: 10.1016/j.neuron.2018.07.051. View

Pezze M, Feldon J . Mesolimbic dopaminergic pathways in fear conditioning. Prog Neurobiol. 2004; 74(5):301-20. DOI: 10.1016/j.pneurobio.2004.09.004. View

Chen Q, Veenman L, Knopp K, Yan Z, Medina L, Song W . Evidence for the preferential localization of glutamate receptor-1 subunits of AMPA receptors to the dendritic spines of medium spiny neurons in rat striatum. Neuroscience. 1998; 83(3):749-61. DOI: 10.1016/s0306-4522(97)00452-1. View

Albin R, Young A, Penney J . The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989; 12(10):366-75. DOI: 10.1016/0166-2236(89)90074-x. View

Foster D, Wilson J, Remke D, Mahmood M, Uddin M, Wess J . Antipsychotic-like Effects of M4 Positive Allosteric Modulators Are Mediated by CB2 Receptor-Dependent Inhibition of Dopamine Release. Neuron. 2016; 91(6):1244-1252. PMC: 5033724. DOI: 10.1016/j.neuron.2016.08.017. View

Stuber G, Sparta D, Stamatakis A, van Leeuwen W, Hardjoprajitno J, Cho S . Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature. 2011; 475(7356):377-80. PMC: 3775282. DOI: 10.1038/nature10194. View

Jordan C, Xi Z . Progress in brain cannabinoid CB receptor research: From genes to behavior. Neurosci Biobehav Rev. 2019; 98:208-220. PMC: 6401261. DOI: 10.1016/j.neubiorev.2018.12.026. View

Pennartz C, Ito R, Verschure P, Battaglia F, Robbins T . The hippocampal-striatal axis in learning, prediction and goal-directed behavior. Trends Neurosci. 2011; 34(10):548-59. DOI: 10.1016/j.tins.2011.08.001. View

Knopfel T, Song C . Optical voltage imaging in neurons: moving from technology development to practical tool. Nat Rev Neurosci. 2019; 20(12):719-727. DOI: 10.1038/s41583-019-0231-4. View

10.

Araque A, Castillo P, Manzoni O, Tonini R . Synaptic functions of endocannabinoid signaling in health and disease. Neuropharmacology. 2017; 124:13-24. PMC: 5662005. DOI: 10.1016/j.neuropharm.2017.06.017. View

11.

Barrientos C, Knowland D, Wu M, Lilascharoen V, Huang K, Malenka R . Cocaine-Induced Structural Plasticity in Input Regions to Distinct Cell Types in Nucleus Accumbens. Biol Psychiatry. 2018; 84(12):893-904. PMC: 8169057. DOI: 10.1016/j.biopsych.2018.04.019. View

12.

Mateo Y, Johnson K, Covey D, Atwood B, Wang H, Zhang S . Endocannabinoid Actions on Cortical Terminals Orchestrate Local Modulation of Dopamine Release in the Nucleus Accumbens. Neuron. 2017; 96(5):1112-1126.e5. PMC: 5728656. DOI: 10.1016/j.neuron.2017.11.012. View

13.

Gerfen C, Surmeier D . Modulation of striatal projection systems by dopamine. Annu Rev Neurosci. 2011; 34:441-66. PMC: 3487690. DOI: 10.1146/annurev-neuro-061010-113641. View

14.

Tepper J, Koos T, Ibanez-Sandoval O, Tecuapetla F, Faust T, Assous M . Heterogeneity and Diversity of Striatal GABAergic Interneurons: Update 2018. Front Neuroanat. 2018; 12:91. PMC: 6235948. DOI: 10.3389/fnana.2018.00091. View

15.

Yavas E, Young A . N-Methyl-d-aspartate Modulation of Nucleus Accumbens Dopamine Release by Metabotropic Glutamate Receptors: Fast Cyclic Voltammetry Studies in Rat Brain Slices in Vitro. ACS Chem Neurosci. 2017; 8(2):320-328. DOI: 10.1021/acschemneuro.6b00397. View

16.

ODonnell P, Greene J, Pabello N, Lewis B, Grace A . Modulation of cell firing in the nucleus accumbens. Ann N Y Acad Sci. 1999; 877:157-75. DOI: 10.1111/j.1749-6632.1999.tb09267.x. View

17.

Wang H, Jing M, Li Y . Lighting up the brain: genetically encoded fluorescent sensors for imaging neurotransmitters and neuromodulators. Curr Opin Neurobiol. 2018; 50:171-178. PMC: 5984720. DOI: 10.1016/j.conb.2018.03.010. View

18.

Ungerstedt U . 6-hydroxydopamine-induced degeneration of the nigrostriatal dopamine pathway: the turning syndrome. Pharmacol Ther B. 1976; 2(1):37-40. DOI: 10.1016/0306-039x(76)90016-7. View

19.

Klawonn A, Malenka R . Nucleus Accumbens Modulation in Reward and Aversion. Cold Spring Harb Symp Quant Biol. 2019; 83:119-129. PMC: 6650377. DOI: 10.1101/sqb.2018.83.037457. View

20.

Airan R, Thompson K, Fenno L, Bernstein H, Deisseroth K . Temporally precise in vivo control of intracellular signalling. Nature. 2009; 458(7241):1025-9. DOI: 10.1038/nature07926. View