title: Voltage drives diverse endocannabinoid signals to mediate striatal microcircuit-specific plasticity.
abstract: The dorsolateral striatum and cannabinoid type 1 receptor (CB1) signaling mediate habitual action learning, which is thought to require a balance of activity in the direct and indirect striatal output pathways. However, very little is known about how the high CB1-expressing striatal inhibitory microcircuitry might contribute to long-term plasticity capable of sculpting direct and indirect pathway output. Using optogenetic and molecular interrogation of striatal GABAergic microcircuits, we examined voltage-dependent long-term depression of inhibitory synapses (iLTD) onto mouse and rat medium spiny projection neurons (MSNs). The observed iLTD involved recruitment of different endocannabinoid types and showed both presynaptic and postsynaptic selectivity for MSN subtypes, ultimately resulting in a powerful disinhibition of direct pathway MSNs. These results suggest a new role for voltage states in gating circuit-specific forms of synaptic plasticity and illuminate possible circuit dynamics underlying action control.
authors.affiliation: Section on Synaptic Pharmacology, Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism, US National Institutes of Health, Bethesda, Maryland, USA.
authors.forename: Brian N
authors.initials: BN
authors.lastname: Mathur
authors.forename: Chiyoko
authors.initials: C
authors.lastname: Tanahira
authors.forename: Nobuaki
authors.initials: N
authors.lastname: Tamamaki
authors.forename: David M
authors.initials: DM
authors.lastname: Lovinger
mesh_terms: D000779:Anesthetics, Local / Q000494:pharmacology; D000818:Animals; D000831:Animals, Newborn; D003342:Corpus Striatum / Q000166:cytology* / Q000187:drug effects / Q000502:physiology; D004791:Enzyme Inhibitors; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects / Q000502:physiology; D005260:Female; D049452:Green Fluorescent Proteins / Q000235:genetics; D066298:In Vitro Techniques; D008012:Lidocaine / Q000031:analogs & derivatives / Q000494:pharmacology; D008297:Male; D049990:Membrane Transport Modulators; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D009473:Neuronal Plasticity / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D010320:Parvalbumins / Q000235:genetics; D020710:RGS Proteins / Q000235:genetics; D051381:Rats; D017207:Rats, Sprague-Dawley; D043884:Receptor, Cannabinoid, CB1 / Q000378:metabolism*; D015398:Signal Transduction / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D013569:Synapses / Q000187:drug effects / Q000502:physiology*; D050916:TRPV Cation Channels / Q000172:deficiency
chemical_list: D000779:Anesthetics, Local; D004791:Enzyme Inhibitors; D049990:Membrane Transport Modulators; D010320:Parvalbumins; D020710:RGS Proteins; D043884:Receptor, Cannabinoid, CB1; D050916:TRPV Cation Channels; C493921:TRPV1 protein, mouse; C116925:regulator of g-protein signaling 9; D049452:Green Fluorescent Proteins; C012647:QX-314; D008012:Lidocaine
references.citation: Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9371-6
references.pmid: 11470906
references.citation: J Neurosci. 2009 Feb 4;29(5):1375-80
references.pmid: 19193884
references.citation: Proc Biol Sci. 1998 Nov 7;265(1410):2081-5
references.pmid: 9842734
references.citation: J Neurosci. 2005 Jul 20;25(29):6826-35
references.pmid: 16033892
references.citation: Neuroscience. 2003;119(2):481-96
references.pmid: 12770562
references.citation: Learn Mem. 2004 Jul-Aug;11(4):459-63
references.pmid: 15286184
references.citation: J Comp Neurol. 1980 Dec 1;194(3):599-615
references.pmid: 7451684
references.citation: J Neurosci. 1993 Mar;13(3):900-13
references.pmid: 8441015
references.citation: Front Integr Neurosci. 2007 Nov 02;1:6
references.pmid: 18958234
references.citation: Neuron. 2004 Oct 28;44(3):483-93
references.pmid: 15504328
references.citation: J Neurosci. 2004 Sep 8;24(36):7916-22
references.pmid: 15356204
references.citation: Trends Neurosci. 1989 Oct;12(10):366-75
references.pmid: 2479133
references.citation: J Neurophysiol. 2006 Feb;95(2):1285-90
references.pmid: 16251264
references.citation: Neuron. 2012 Jan 26;73(2):347-59
references.pmid: 22284188
references.citation: Neurosci Lett. 2008 Apr 18;435(2):90-4
references.pmid: 18358609
references.citation: Arch Neurol. 2003 Oct;60(10):1365-8
references.pmid: 14568805
references.citation: Annu Rev Neurosci. 2011;34:441-66
references.pmid: 21469956
references.citation: J Comp Neurol. 2008 Feb 1;506(4):604-15
references.pmid: 18067139
references.citation: Nat Neurosci. 1999 May;2(5):467-72
references.pmid: 10321252
references.citation: Neuron. 2010 Feb 11;65(3):320-7
references.pmid: 20159446
references.citation: Nature. 1998 Jul 30;394(6692):475-8
references.pmid: 9697769
references.citation: J Neurosci. 2007 Apr 4;27(14):3663-76
references.pmid: 17409230
references.citation: Brain Res. 1990 Dec 17;536(1-2):1-15
references.pmid: 2085740
references.citation: Prog Brain Res. 2007;160:91-110
references.pmid: 17499110
references.citation: J Neurosci. 2001 Aug 15;21(16):5944-51
references.pmid: 11487617
references.citation: Neurosci Lett. 1998 Oct 2;254(3):137-40
references.pmid: 10214976
references.citation: Trends Neurosci. 2004 Nov;27(11):662-9
references.pmid: 15474166
references.citation: J Neurosci. 2011 May 18;31(20):7402-11
references.pmid: 21593324
references.citation: Nat Neurosci. 2011 Nov 06;14(12):1542-7
references.pmid: 22057189
references.citation: Science. 2003 Oct 3;302(5642):84-8
references.pmid: 14526074
references.citation: Neuroscience. 1994 Oct;62(3):707-19
references.pmid: 7870301
references.citation: J Neurosci. 2000 Jan 1;20(1):375-86
references.pmid: 10627614
references.citation: Proc Natl Acad Sci U S A. 2012 Oct 2;109(40):E2717-25
references.pmid: 23012412
references.citation: Proc Natl Acad Sci U S A. 2006 Oct 10;103(41):15254-9
references.pmid: 17015831
references.citation: Eur J Neurosci. 2006 Oct;24(8):2246-52
references.pmid: 17042791
references.citation: J Neurosci. 2006 May 3;26(18):4740-51
references.pmid: 16672646
references.citation: Science. 2000 Apr 14;288(5464):306-13
references.pmid: 10764638
references.citation: J Neurosci. 2006 Nov 29;26(48):12587-95
references.pmid: 17135420
references.citation: Neuroscience. 2008 Mar 3;152(1):265-72
references.pmid: 18082330
references.citation: J Neurosci. 1998 Jan 1;18(1):266-83
references.pmid: 9412506
references.citation: J Neurosci. 2007 Jun 20;27(25):6781-7
references.pmid: 17581965
references.citation: J Physiol. 2006 Sep 15;575(Pt 3):789-806
references.pmid: 16825300
references.citation: J Neurochem. 2003 May;85(4):1018-25
references.pmid: 12716433
references.citation: J Neurosci. 2012 Sep 26;32(39):13411-20
references.pmid: 23015432
references.citation: Nat Neurosci. 2008 Feb;11(2):152-9
references.pmid: 18204441
references.citation: J Neurosci. 1996 Apr 1;16(7):2397-410
references.pmid: 8601819
references.citation: Neurosci Res. 2009 Mar;63(3):213-23
references.pmid: 19167436
references.citation: Trends Neurosci. 2003 Aug;26(8):436-43
references.pmid: 12900175
references.citation: Nature. 2013 Feb 14;494(7436):238-42
references.pmid: 23354054
references.citation: J Anat. 2000 May;196 ( Pt 4):527-42
references.pmid: 10923985