Chronic nicotine impairs sparse motor learning via striatal fast-spiking parvalbumin interneurons.
Action Potentials
Animals
Anxiety
/ physiopathology
Corpus Striatum
/ drug effects
Designer Drugs
/ pharmacology
Interneurons
/ drug effects
Locomotion
/ physiology
Male
Mice
Mice, Inbred C57BL
Motor Activity
/ physiology
Nicotine
/ pharmacology
Parvalbumins
/ metabolism
Substance Withdrawal Syndrome
/ metabolism
dorsal striatum
extracellular single-unit recording
fast-spiking interneurons
local field potential
motor learning
nicotine withdrawal
Journal
Addiction biology
ISSN: 1369-1600
Titre abrégé: Addict Biol
Pays: United States
ID NLM: 9604935
Informations de publication
Date de publication:
05 2021
05 2021
Historique:
revised:
09
07
2020
received:
28
03
2020
accepted:
21
07
2020
pubmed:
9
8
2020
medline:
3
11
2021
entrez:
9
8
2020
Statut:
ppublish
Résumé
Nicotine can diversely affect neural activity and motor learning in animals. However, the impact of chronic nicotine on striatal activity in vivo and motor learning at long-term sparse timescale remains unknown. Here, we demonstrate that chronic nicotine persistently suppresses the activity of striatal fast-spiking parvalbumin interneurons, which mediate nicotine-induced deficit in sparse motor learning. Six weeks of longitudinal in vivo single-unit recording revealed that mice show reduced activity of fast-spiking interneurons in the dorsal striatum during chronic nicotine exposure and withdrawal. The reduced firing of fast-spiking interneurons was accompanied by spike broadening, diminished striatal delta oscillation power, and reduced sample entropy in local field potential. In addition, chronic nicotine withdrawal impaired motor learning with a weekly sparse training regimen but did not affect general locomotion and anxiety-like behavior. Lastly, the excitatory DREADD hM3Dq-mediated activation of striatal fast-spiking parvalbumin interneurons reversed the chronic nicotine withdrawal-induced deficit in sparse motor learning. Taken together, we identified that chronic nicotine withdrawal impairs sparse motor learning via disruption of activity in striatal fast-spiking parvalbumin interneurons. These findings suggest that sparse motor learning paradigm can reveal the subtle effect of nicotine withdrawal on motor function and that striatal fast-spiking parvalbumin interneurons are a neural substrate of nicotine's effect on motor learning.
Identifiants
pubmed: 32767546
doi: 10.1111/adb.12956
pmc: PMC8243919
doi:
Substances chimiques
Designer Drugs
0
Parvalbumins
0
Nicotine
6M3C89ZY6R
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e12956Informations de copyright
© 2020 The Authors. Addiction Biology published by John Wiley & Sons Ltd on behalf of Society for the Study of Addiction.
Références
Psychopharmacology (Berl). 1994 Dec;116(4):407-13
pubmed: 7701041
Neuropsychopharmacology. 2017 Nov;42(12):2314-2324
pubmed: 28462940
Eur Neuropsychopharmacol. 2010 Jun;20(6):369-78
pubmed: 20189358
Neuroscience. 2005;131(1):1-11
pubmed: 15680687
Neuron. 2012 Jan 12;73(1):159-70
pubmed: 22243754
Neuroimage. 2012 Aug 1;62(1):290-9
pubmed: 22569545
Addict Behav. 2017 Nov;74:90-97
pubmed: 28600927
Neuropsychopharmacology. 2012 Nov;37(12):2661-70
pubmed: 22828747
Behav Brain Res. 2001 Nov 1;125(1-2):65-73
pubmed: 11682095
Neural Comput. 2004 Aug;16(8):1661-87
pubmed: 15228749
Pharmacol Biochem Behav. 2010 Jun;95(4):466-72
pubmed: 20347863
J Neuroinflammation. 2016 May 16;13(1):110
pubmed: 27184631
Neuron. 2017 Mar 22;93(6):1451-1463.e4
pubmed: 28334608
Front Neuroanat. 2018 Nov 08;12:91
pubmed: 30467465
Cell Rep. 2018 Aug 21;24(8):2179-2190.e7
pubmed: 30134177
Nicotine Tob Res. 2007 Mar;9(3):315-27
pubmed: 17365764
Nat Commun. 2017 Apr 06;8:15039
pubmed: 28382952
J Neurosci. 2010 Jul 21;30(29):9877-89
pubmed: 20660270
J Neurosci. 2009 Oct 7;29(40):12428-39
pubmed: 19812319
Neuron. 2019 Feb 6;101(3):444-458.e6
pubmed: 30658860
Curr Biol. 2013 Dec 2;23(23):2327-35
pubmed: 24239118
Eur J Neurosci. 2009 Sep;30(5):848-59
pubmed: 19659455
J Neurophysiol. 2002 Apr;87(4):2190-4
pubmed: 11929936
Cell Death Differ. 2010 Jul;17(7):1104-14
pubmed: 19960023
J Comput Neurosci. 2012 Dec;33(3):547-58
pubmed: 22648379
Trends Neurosci. 2003 Mar;26(3):161-7
pubmed: 12591219
Neurobiol Learn Mem. 2018 Sep;153(Pt A):79-91
pubmed: 29778763
Brain Res Mol Brain Res. 2000 Dec 28;85(1-2):234-8
pubmed: 11146126
J Pharmacol Exp Ther. 2003 Nov;307(2):526-34
pubmed: 12970387
J Neurochem. 1988 Apr;50(4):1123-30
pubmed: 3346670
Clin Neurophysiol. 2011 Dec;122(12):2375-83
pubmed: 21641861
eNeuro. 2016 Feb 02;3(1):
pubmed: 26866057
Addict Biol. 2017 Sep;22(5):1205-1217
pubmed: 27126842
Neurosci Lett. 2001 Dec 4;316(1):9-12
pubmed: 11720766
Neuron. 2000 Dec;28(3):927-39
pubmed: 11163277
Brain Res. 1981 Dec 28;230(1-2):346-50
pubmed: 7317783
Front Hum Neurosci. 2013 Jan 09;6:343
pubmed: 23316151
Brain Res. 2001 Mar 16;894(2):347-53
pubmed: 11251214
Nat Neurosci. 2009 Dec;12(12):1577-85
pubmed: 19881502
Neuron. 2010 Aug 12;67(3):466-79
pubmed: 20696383
Brain Res. 1980 Feb 10;183(2):253-63
pubmed: 7353139
Neuropsychopharmacology. 2016 Dec;41(13):3051-3059
pubmed: 27388328
Psychopharmacology (Berl). 2007 Feb;190(3):269-319
pubmed: 16896961
Neurosci Lett. 2008 Jul 11;439(2):187-91
pubmed: 18524488
EMBO J. 2012 Feb 1;31(3):640-53
pubmed: 22068054
Neurobiol Learn Mem. 2004 May;81(3):211-6
pubmed: 15082022
J Pharmacol Exp Ther. 1983 Sep;226(3):817-25
pubmed: 6887012
Curr Opin Neurobiol. 2000 Dec;10(6):732-9
pubmed: 11240282
Exp Neurol. 2020 Apr;326:113206
pubmed: 31962128
Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2875-80
pubmed: 10688892
Neuropharmacology. 2001 Aug;41(2):272-81
pubmed: 11489464
Sci Rep. 2015 Nov 17;5:16742
pubmed: 26572101
Front Neurosci. 2010 Sep 15;4:300
pubmed: 21350600
Psychopharmacology (Berl). 2005 Jun;179(4):863-72
pubmed: 15619104
Sci Rep. 2018 Mar 1;8(1):3840
pubmed: 29497149
J Neurosci. 2014 Feb 19;34(8):2845-59
pubmed: 24553926
J Neurophysiol. 1999 Oct;82(4):1855-64
pubmed: 10515974
Front Cell Neurosci. 2015 Jan 14;8:460
pubmed: 25642167
Cell. 2018 Feb 8;172(4):683-695.e15
pubmed: 29425490
Neuron. 2017 Oct 11;96(2):267-284
pubmed: 29024654
Psychopharmacology (Berl). 2014 Nov;231(22):4371-81
pubmed: 24752658
Nat Commun. 2016 Jul 06;7:12102
pubmed: 27381274
J Neurosci. 2005 Apr 13;25(15):3857-69
pubmed: 15829638
Neuropsychopharmacology. 2018 Apr;43(5):934-936
pubmed: 29303143
Front Pharmacol. 2012 Oct 08;3:180
pubmed: 23060798
Proc Natl Acad Sci U S A. 2012 Oct 30;109(44):18126-31
pubmed: 23074253
Hippocampus. 2014 Nov;24(11):1300-7
pubmed: 24909986
J Neurosci. 2002 Mar 1;22(5):1499-512
pubmed: 11880480
Neurosurgery. 2012 Oct;71(4):885-91
pubmed: 22743360
J Neurosci. 2010 Feb 10;30(6):2223-34
pubmed: 20147549
Mov Disord. 2015 Jul;30(8):1014-25
pubmed: 26095280
J Neurosci. 1993 Nov;13(11):4908-23
pubmed: 7693897
Behav Genet. 2012 Jan;42(1):133-50
pubmed: 21822688
Nat Rev Neurosci. 2007 Jun;8(6):451-65
pubmed: 17514198
Front Syst Neurosci. 2011 Jun 20;5:45
pubmed: 21743805
Clin Neurophysiol. 2005 Aug;116(8):1826-34
pubmed: 15979403
Addict Biol. 2021 May;26(3):e12956
pubmed: 32767546
Proc Natl Acad Sci U S A. 2006 Oct 10;103(41):15254-9
pubmed: 17015831
Drug Alcohol Depend. 2012 Mar 1;121(3):240-6
pubmed: 21945235
J Neurosci. 2002 Jan 15;22(2):529-35
pubmed: 11784799
Science. 2001 Aug 10;293(5532):1159-63
pubmed: 11498596
Neuroscience. 2016 Jun 2;324:321-9
pubmed: 26968763
Trends Neurosci. 2012 Sep;35(9):557-64
pubmed: 22858522
J Neurosci. 2012 Feb 15;32(7):2352-6
pubmed: 22396410
J Physiol. 2013 Jan 1;591(1):203-17
pubmed: 23045343
Proc Natl Acad Sci U S A. 2012 Feb 21;109(8):3101-6
pubmed: 22308372
Nature. 2012 Aug 16;488(7411):379-83
pubmed: 22878719
J Neurosci. 2016 May 11;36(19):5228-40
pubmed: 27170121
Behav Brain Res. 1997 Sep;87(2):233-8
pubmed: 9331492
Psychopharmacology (Berl). 2011 Oct;217(3):353-65
pubmed: 21487656
Nat Commun. 2014 May 21;5:3925
pubmed: 24968237
Br J Pharmacol. 2015 Jun;172(11):2864-77
pubmed: 25625469
Neurobiol Learn Mem. 2012 May;97(4):482-94
pubmed: 22521799
Sens Actuators A Phys. 2009 Dec 1;156(2):388-393
pubmed: 21379404
Eur J Pharmacol. 2000 Mar 30;393(1-3):51-8
pubmed: 10770997
J Neurophysiol. 2004 Jul;92(1):600-8
pubmed: 15056678
Biol Psychiatry. 2017 Aug 1;82(3):194-203
pubmed: 28347488
Neuron. 2014 Apr 2;82(1):63-70
pubmed: 24613418
J Neurochem. 1994 Jul;63(1):186-94
pubmed: 7911509