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Articles, Behavioral/Cognitive

Phasic Dopamine Release in the Nucleus Accumbens in Response to Pro-Social 50 kHz Ultrasonic Vocalizations in Rats

Ingo Willuhn, Amanda Tose, Matthew J. Wanat, Andrew S. Hart, Nick G. Hollon, Paul E.M. Phillips, Rainer K.W. Schwarting and Markus Wöhr
Journal of Neuroscience 6 August 2014, 34 (32) 10616-10623; DOI: https://doi.org/10.1523/JNEUROSCI.1060-14.2014
Ingo Willuhn
1Departments of Psychiatry and Behavioral Sciences and Pharmacology, University of Washington, Seattle, Washington 98195 and
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Amanda Tose
1Departments of Psychiatry and Behavioral Sciences and Pharmacology, University of Washington, Seattle, Washington 98195 and
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Matthew J. Wanat
1Departments of Psychiatry and Behavioral Sciences and Pharmacology, University of Washington, Seattle, Washington 98195 and
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Andrew S. Hart
1Departments of Psychiatry and Behavioral Sciences and Pharmacology, University of Washington, Seattle, Washington 98195 and
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Nick G. Hollon
1Departments of Psychiatry and Behavioral Sciences and Pharmacology, University of Washington, Seattle, Washington 98195 and
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Paul E.M. Phillips
1Departments of Psychiatry and Behavioral Sciences and Pharmacology, University of Washington, Seattle, Washington 98195 and
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Rainer K.W. Schwarting
2Behavioral Neuroscience, Experimental and Biological Psychology, Faculty of Psychology, Philipps-University of Marburg, 35032 Marburg, Germany
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Markus Wöhr
2Behavioral Neuroscience, Experimental and Biological Psychology, Faculty of Psychology, Philipps-University of Marburg, 35032 Marburg, Germany
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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.

  • dopamine
  • fast-scan cyclic voltammetry
  • nucleus accumbens
  • social behavior
  • ultrasonic communication
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The Journal of Neuroscience: 34 (32)
Journal of Neuroscience
Vol. 34, Issue 32
6 Aug 2014
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Phasic Dopamine Release in the Nucleus Accumbens in Response to Pro-Social 50 kHz Ultrasonic Vocalizations in Rats
Ingo Willuhn, Amanda Tose, Matthew J. Wanat, Andrew S. Hart, Nick G. Hollon, Paul E.M. Phillips, Rainer K.W. Schwarting, Markus Wöhr
Journal of Neuroscience 6 August 2014, 34 (32) 10616-10623; DOI: 10.1523/JNEUROSCI.1060-14.2014

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Phasic Dopamine Release in the Nucleus Accumbens in Response to Pro-Social 50 kHz Ultrasonic Vocalizations in Rats
Ingo Willuhn, Amanda Tose, Matthew J. Wanat, Andrew S. Hart, Nick G. Hollon, Paul E.M. Phillips, Rainer K.W. Schwarting, Markus Wöhr
Journal of Neuroscience 6 August 2014, 34 (32) 10616-10623; DOI: 10.1523/JNEUROSCI.1060-14.2014
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Keywords

  • dopamine
  • fast-scan cyclic voltammetry
  • nucleus accumbens
  • social behavior
  • ultrasonic communication

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