title: Phasic dopamine release in the nucleus accumbens in response to pro-social 50 kHz ultrasonic vocalizations in rats.
abstract: Rats emit ultrasonic vocalizations (USVs) that are thought to serve as situation-dependent affective signals and accomplish important communicative functions. In appetitive situations, rats produce 50 kHz USVs, whereas 22 kHz USVs occur in aversive situations. Reception of 50 kHz USVs induces social approach behavior, while 22 kHz USVs lead to freezing behavior. These opposite behavioral responses are paralleled by distinct brain activation patterns, with 50 kHz USVs, but not 22 kHz USVs, activating neurons in the nucleus accumbens (NAcc). The NAcc mediates appetitive behavior and is critically modulated by dopaminergic afferents that are known to encode the value of reward. Therefore, we hypothesized that 50 kHz USVs, but not 22 kHz USVs, elicit NAcc dopamine release. While recording dopamine signaling with fast-scan cyclic voltammetry, freely moving rats were exposed to playback of four acoustic stimuli via an ultrasonic speaker in random order: (1) 50 kHz USVs, (2) 22 kHz USVs, (3) time- and amplitude-matched white noise, and (4) background noise. Only presentation of 50 kHz USVs induced phasic dopamine release and elicited approach behavior toward the speaker. Both of these effects, neurochemical and behavioral, were most pronounced during initial playback, but then declined rapidly with subsequent presentations, indicating a close temporal relationship between the two measures. Moreover, the magnitudes of these effects during initial playback were significantly correlated. Collectively, our findings show that NAcc dopamine release encodes pro-social 50 kHz USVs, but not alarming 22 kHz USVs. Thus, our results support the hypothesis that these call types are processed in distinct neuroanatomical regions and establish a functional link between pro-social communicative signals and reward-related neurotransmission.
authors.affiliation: Departments of Psychiatry and Behavioral Sciences and Pharmacology, University of Washington, Seattle, Washington 98195 and ingo.willuhn@gmail.com markus.woehr@staff.uni-marburg.de.
authors.forename: Ingo
authors.initials: I
authors.lastname: Willuhn
authors.affiliation: Departments of Psychiatry and Behavioral Sciences and Pharmacology, University of Washington, Seattle, Washington 98195 and.
authors.forename: Amanda
authors.initials: A
authors.lastname: Tose
authors.affiliation: Departments of Psychiatry and Behavioral Sciences and Pharmacology, University of Washington, Seattle, Washington 98195 and.
authors.forename: Matthew J
authors.initials: MJ
authors.lastname: Wanat
authors.affiliation: Departments of Psychiatry and Behavioral Sciences and Pharmacology, University of Washington, Seattle, Washington 98195 and.
authors.forename: Andrew S
authors.initials: AS
authors.lastname: Hart
authors.affiliation: Departments of Psychiatry and Behavioral Sciences and Pharmacology, University of Washington, Seattle, Washington 98195 and.
authors.forename: Nick G
authors.initials: NG
authors.lastname: Hollon
authors.affiliation: Departments of Psychiatry and Behavioral Sciences and Pharmacology, University of Washington, Seattle, Washington 98195 and.
authors.forename: Paul E M
authors.initials: PE
authors.lastname: Phillips
authors.affiliation: Behavioral Neuroscience, Experimental and Biological Psychology, Faculty of Psychology, Philipps-University of Marburg, 35032 Marburg, Germany.
authors.forename: Rainer K W
authors.initials: RK
authors.lastname: Schwarting
authors.affiliation: Behavioral Neuroscience, Experimental and Biological Psychology, Faculty of Psychology, Philipps-University of Marburg, 35032 Marburg, Germany ingo.willuhn@gmail.com markus.woehr@staff.uni-marburg.de.
authors.forename: Markus
authors.initials: M
authors.lastname: Wöhr
mesh_terms: D000161:Acoustic Stimulation; D000818:Animals; D001070:Appetitive Behavior; D004298:Dopamine / Q000378:metabolism*; D004563:Electrochemistry; D009714:Nucleus Accumbens / Q000378:metabolism*; D009949:Orientation; D011601:Psychophysics; D051381:Rats; D012919:Social Behavior; D013057:Spectrum Analysis; D014465:Ultrasonics; D014828:Vocalization, Animal / Q000502:physiology*
chemical_list: D004298:Dopamine
keywords: dopamine; fast-scan cyclic voltammetry; nucleus accumbens; social behavior; ultrasonic communication
references.citation: Psychopharmacology (Berl). 2010 Sep;211(4):435-42
references.pmid: 20571780
references.citation: Neurosci Biobehav Rev. 1999 May;23(5):743-60
references.pmid: 10392663
references.citation: Behav Brain Res. 2007 Sep 4;182(2):290-300
references.pmid: 17452055
references.citation: Nat Methods. 2010 Feb;7(2):126-9
references.pmid: 20037591
references.citation: Pharmacol Biochem Behav. 2009 Dec;94(2):285-95
references.pmid: 19758572
references.citation: J Comp Psychol. 1998 Mar;112(1):65-73
references.pmid: 9528115
references.citation: Neurosci Lett. 2008 Apr 11;435(1):17-23
references.pmid: 18328625
references.citation: PLoS One. 2007 Dec 26;2(12):e1365
references.pmid: 18159248
references.citation: Cell Tissue Res. 2013 Oct;354(1):81-97
references.pmid: 23576070
references.citation: Neurosci Biobehav Rev. 2002 May;26(3):321-52
references.pmid: 12034134
references.citation: Behav Brain Res. 1994 Dec 15;65(2):221-9
references.pmid: 7718155
references.citation: Science. 1997 Mar 14;275(5306):1593-9
references.pmid: 9054347
references.citation: Curr Opin Neurobiol. 2013 Jun;23(3):310-7
references.pmid: 23375168
references.citation: J Neurosci. 2002 Dec 1;22(23):10477-86
references.pmid: 12451147
references.citation: Psychopharmacology (Berl). 2013 Feb;225(4):853-68
references.pmid: 23052567
references.citation: Psychopharmacology (Berl). 2007 Apr;191(3):461-82
references.pmid: 17225164
references.citation: J Am Assoc Lab Anim Sci. 2007 Jan;46(1):28-34
references.pmid: 17203913
references.citation: Physiol Behav. 1991 Nov;50(5):967-72
references.pmid: 1805287
references.citation: Psychopharmacology (Berl). 2013 Oct;229(4):687-700
references.pmid: 23700082
references.citation: J Pharmacol Exp Ther. 1997 Jul;282(1):318-25
references.pmid: 9223570
references.citation: Behav Brain Res. 2007 Sep 4;182(2):274-83
references.pmid: 17449117
references.citation: Psychopharmacology (Berl). 2014 Jul;231(13):2567-77
references.pmid: 24414610
references.citation: Proc Natl Acad Sci U S A. 2012 Dec 11;109(50):20703-8
references.pmid: 23184975
references.citation: Behav Brain Res. 2006 Mar 15;168(1):64-73
references.pmid: 16343652
references.citation: Prog Neurobiol. 1980;14(2-3):69-97
references.pmid: 6999537
references.citation: J Comp Psychol. 2011 May;125(2):250-3
references.pmid: 21341907
references.citation: Behav Brain Res. 2007 Dec 28;185(2):69-75
references.pmid: 17714801
references.citation: Dev Psychobiol. 1987 Jan;20(1):39-55
references.pmid: 3556783
references.citation: Nature. 2011 Jan 6;469(7328):53-7
references.pmid: 21150898
references.citation: J Neurosci. 2010 Dec 8;30(49):16585-600
references.pmid: 21147998
references.citation: Int Rev Neurobiol. 1982;23:303-65
references.pmid: 6749738
references.citation: J Comp Psychol. 2002 Mar;116(1):73-82
references.pmid: 11926686
references.citation: Behav Neurosci. 2001 Aug;115(4):940-4
references.pmid: 11508733
references.citation: Annu Rev Neurosci. 2000;23:155-84
references.pmid: 10845062
references.citation: Nat Neurosci. 2007 Aug;10(8):1020-8
references.pmid: 17603481
references.citation: Behav Brain Res. 2012 Jan 1;226(1):77-86
references.pmid: 21911010
references.citation: Neurobiol Learn Mem. 2012 Sep;98(2):154-64
references.pmid: 22677211