Amygdalar auditory neurons contribute to self-other distinction during ultrasonic social vocalization in rats

Although clinical studies reported hyperactivation of the auditory system and amygdala in patients with auditory hallucinations (hearing others’ but not one’s own voice, independent of any external stimulus), neural mechanisms of self/other attribution is not well understood. We recorded neuronal re...

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Main Authors: Jumpei Matsumoto, Hiroshi Nishimaru, Yusaku Takamura, Susumu Urakawa, Taketoshi Ono, Hisao Nishijo
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-09-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fnins.2016.00399/full
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author Jumpei Matsumoto
Hiroshi Nishimaru
Yusaku Takamura
Susumu Urakawa
Taketoshi Ono
Hisao Nishijo
author_facet Jumpei Matsumoto
Hiroshi Nishimaru
Yusaku Takamura
Susumu Urakawa
Taketoshi Ono
Hisao Nishijo
author_sort Jumpei Matsumoto
collection DOAJ
description Although clinical studies reported hyperactivation of the auditory system and amygdala in patients with auditory hallucinations (hearing others’ but not one’s own voice, independent of any external stimulus), neural mechanisms of self/other attribution is not well understood. We recorded neuronal responses in the dorsal amygdala including the lateral amygdaloid nucleus to ultrasonic vocalization (USVs) emitted by subjects and conspecifics during free social interaction in 16 adult male rats. The animals emitting the USVs were identified by EMG recordings. One-quarter of the amygdalar neurons (15/60) responded to 50 kHz calls by the subject and/or conspecifics. Among the responsive neurons, most neurons (Type-Other neurons) (73%, 11/15) responded only to calls by conspecifics but not subjects. Two Type-Self neurons (13%, 2/15) responded to calls by the subject but not those by conspecifics, although their response selectivity to subjects vs. conspecifics was lower than that of Type-Other neurons. The remaining two neurons (13%) responded to calls by both the subject and conspecifics. Furthermore, population coding of the amygdalar neurons represented distinction of subject vs. conspecific calls. The present results provide the first neurophysiological evidence that the amygdala discriminately represents affective social calls by subject and conspecifics. These findings suggest that the amygdala is an important brain region for self/other attribution. Furthermore, pathological activation of the amygdala, where Type-Other neurons predominate, could induce external misattribution of percepts of vocalization.
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spelling doaj.art-0c01cec1c7214b57b550d8f007acefde2022-12-21T19:13:18ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2016-09-011010.3389/fnins.2016.00399208019Amygdalar auditory neurons contribute to self-other distinction during ultrasonic social vocalization in ratsJumpei Matsumoto0Hiroshi Nishimaru1Yusaku Takamura2Susumu Urakawa3Taketoshi Ono4Hisao Nishijo5University of ToyamaUniversity of ToyamaUniversity of ToyamaUniversity of ToyamaUniversity of ToyamaUniversity of ToyamaAlthough clinical studies reported hyperactivation of the auditory system and amygdala in patients with auditory hallucinations (hearing others’ but not one’s own voice, independent of any external stimulus), neural mechanisms of self/other attribution is not well understood. We recorded neuronal responses in the dorsal amygdala including the lateral amygdaloid nucleus to ultrasonic vocalization (USVs) emitted by subjects and conspecifics during free social interaction in 16 adult male rats. The animals emitting the USVs were identified by EMG recordings. One-quarter of the amygdalar neurons (15/60) responded to 50 kHz calls by the subject and/or conspecifics. Among the responsive neurons, most neurons (Type-Other neurons) (73%, 11/15) responded only to calls by conspecifics but not subjects. Two Type-Self neurons (13%, 2/15) responded to calls by the subject but not those by conspecifics, although their response selectivity to subjects vs. conspecifics was lower than that of Type-Other neurons. The remaining two neurons (13%) responded to calls by both the subject and conspecifics. Furthermore, population coding of the amygdalar neurons represented distinction of subject vs. conspecific calls. The present results provide the first neurophysiological evidence that the amygdala discriminately represents affective social calls by subject and conspecifics. These findings suggest that the amygdala is an important brain region for self/other attribution. Furthermore, pathological activation of the amygdala, where Type-Other neurons predominate, could induce external misattribution of percepts of vocalization.http://journal.frontiersin.org/Journal/10.3389/fnins.2016.00399/fullAmygdalasingle unit recordingauditory hallucinationultrasonic vocalizationself/other attribution
spellingShingle Jumpei Matsumoto
Hiroshi Nishimaru
Yusaku Takamura
Susumu Urakawa
Taketoshi Ono
Hisao Nishijo
Amygdalar auditory neurons contribute to self-other distinction during ultrasonic social vocalization in rats
Frontiers in Neuroscience
Amygdala
single unit recording
auditory hallucination
ultrasonic vocalization
self/other attribution
title Amygdalar auditory neurons contribute to self-other distinction during ultrasonic social vocalization in rats
title_full Amygdalar auditory neurons contribute to self-other distinction during ultrasonic social vocalization in rats
title_fullStr Amygdalar auditory neurons contribute to self-other distinction during ultrasonic social vocalization in rats
title_full_unstemmed Amygdalar auditory neurons contribute to self-other distinction during ultrasonic social vocalization in rats
title_short Amygdalar auditory neurons contribute to self-other distinction during ultrasonic social vocalization in rats
title_sort amygdalar auditory neurons contribute to self other distinction during ultrasonic social vocalization in rats
topic Amygdala
single unit recording
auditory hallucination
ultrasonic vocalization
self/other attribution
url http://journal.frontiersin.org/Journal/10.3389/fnins.2016.00399/full
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