Alterations of the emotional processing system may underlie preserved rapid reaction time in tinnitus

Jake R. Carpenter-Thompson, Kwaku Akrofi, Sara A. Schmidt, Florin Dolcos, Fatima T Husain

Research output: Contribution to journalArticle

Abstract

Although alterations of the limbic system have been linked to tinnitus persistence, the neural networks underlying such alteration are unclear. The present study investigated the effect of tinnitus on emotional processing in middle-aged adults using functional magnetic resonance imaging and stimuli from the International Affective Digital Sounds database. There were three groups of participants: bilateral hearing loss with tinnitus (TIN), age- and gender-matched controls with bilateral hearing loss without tinnitus (HL) and matched normal hearing controls without tinnitus (NH). In the scanner, subjects rated sounds as pleasant, unpleasant, or neutral. The TIN and NH groups, but not the HL group, responded faster to affective sounds compared to neutral sounds. The TIN group had elevated response in bilateral parahippocampus and right insula compared to the NH group, and left parahippocampus compared to HL controls for pleasant relative to neutral sounds. A region-of-interest analysis detected increased activation for NH controls in the right amygdala when responding to affective stimuli, but failed to find a similar heightened response in the TIN and HL groups. All three groups showed increased response in auditory cortices for the affective relative to neutral sounds comparisons. Our results suggest that the emotional processing network is altered in tinnitus to rely on the parahippocampus and insula, rather than the amygdala, and this alteration may maintain a select advantage for the rapid processing of affective stimuli despite the hearing loss. The complex interaction of tinnitus and the limbic system should be accounted for in development of new tinnitus management strategies.

Original languageEnglish (US)
Pages (from-to)28-41
Number of pages14
JournalBrain Research
Volume1567
DOIs
StatePublished - Jun 3 2014

Fingerprint

Tinnitus
Reaction Time
Bilateral Hearing Loss
Limbic System
Amygdala
Auditory Cortex
Hearing Loss
Hearing
Magnetic Resonance Imaging
Databases

Keywords

  • Emotion
  • IADS
  • Tinnitus
  • fMRI

ASJC Scopus subject areas

  • Neuroscience(all)
  • Molecular Biology
  • Clinical Neurology
  • Developmental Biology

Cite this

Alterations of the emotional processing system may underlie preserved rapid reaction time in tinnitus. / Carpenter-Thompson, Jake R.; Akrofi, Kwaku; Schmidt, Sara A.; Dolcos, Florin; Husain, Fatima T.

In: Brain Research, Vol. 1567, 03.06.2014, p. 28-41.

Research output: Contribution to journalArticle

Carpenter-Thompson, Jake R. ; Akrofi, Kwaku ; Schmidt, Sara A. ; Dolcos, Florin ; Husain, Fatima T. / Alterations of the emotional processing system may underlie preserved rapid reaction time in tinnitus. In: Brain Research. 2014 ; Vol. 1567. pp. 28-41.
@article{dc798e830f5f4c2ba80bb8b532887644,
title = "Alterations of the emotional processing system may underlie preserved rapid reaction time in tinnitus",
abstract = "Although alterations of the limbic system have been linked to tinnitus persistence, the neural networks underlying such alteration are unclear. The present study investigated the effect of tinnitus on emotional processing in middle-aged adults using functional magnetic resonance imaging and stimuli from the International Affective Digital Sounds database. There were three groups of participants: bilateral hearing loss with tinnitus (TIN), age- and gender-matched controls with bilateral hearing loss without tinnitus (HL) and matched normal hearing controls without tinnitus (NH). In the scanner, subjects rated sounds as pleasant, unpleasant, or neutral. The TIN and NH groups, but not the HL group, responded faster to affective sounds compared to neutral sounds. The TIN group had elevated response in bilateral parahippocampus and right insula compared to the NH group, and left parahippocampus compared to HL controls for pleasant relative to neutral sounds. A region-of-interest analysis detected increased activation for NH controls in the right amygdala when responding to affective stimuli, but failed to find a similar heightened response in the TIN and HL groups. All three groups showed increased response in auditory cortices for the affective relative to neutral sounds comparisons. Our results suggest that the emotional processing network is altered in tinnitus to rely on the parahippocampus and insula, rather than the amygdala, and this alteration may maintain a select advantage for the rapid processing of affective stimuli despite the hearing loss. The complex interaction of tinnitus and the limbic system should be accounted for in development of new tinnitus management strategies.",
keywords = "Emotion, IADS, Tinnitus, fMRI",
author = "Carpenter-Thompson, {Jake R.} and Kwaku Akrofi and Schmidt, {Sara A.} and Florin Dolcos and Husain, {Fatima T}",
year = "2014",
month = "6",
day = "3",
doi = "10.1016/j.brainres.2014.04.024",
language = "English (US)",
volume = "1567",
pages = "28--41",
journal = "Brain Research",
issn = "0006-8993",
publisher = "Elsevier",

}

TY - JOUR

T1 - Alterations of the emotional processing system may underlie preserved rapid reaction time in tinnitus

AU - Carpenter-Thompson, Jake R.

AU - Akrofi, Kwaku

AU - Schmidt, Sara A.

AU - Dolcos, Florin

AU - Husain, Fatima T

PY - 2014/6/3

Y1 - 2014/6/3

N2 - Although alterations of the limbic system have been linked to tinnitus persistence, the neural networks underlying such alteration are unclear. The present study investigated the effect of tinnitus on emotional processing in middle-aged adults using functional magnetic resonance imaging and stimuli from the International Affective Digital Sounds database. There were three groups of participants: bilateral hearing loss with tinnitus (TIN), age- and gender-matched controls with bilateral hearing loss without tinnitus (HL) and matched normal hearing controls without tinnitus (NH). In the scanner, subjects rated sounds as pleasant, unpleasant, or neutral. The TIN and NH groups, but not the HL group, responded faster to affective sounds compared to neutral sounds. The TIN group had elevated response in bilateral parahippocampus and right insula compared to the NH group, and left parahippocampus compared to HL controls for pleasant relative to neutral sounds. A region-of-interest analysis detected increased activation for NH controls in the right amygdala when responding to affective stimuli, but failed to find a similar heightened response in the TIN and HL groups. All three groups showed increased response in auditory cortices for the affective relative to neutral sounds comparisons. Our results suggest that the emotional processing network is altered in tinnitus to rely on the parahippocampus and insula, rather than the amygdala, and this alteration may maintain a select advantage for the rapid processing of affective stimuli despite the hearing loss. The complex interaction of tinnitus and the limbic system should be accounted for in development of new tinnitus management strategies.

AB - Although alterations of the limbic system have been linked to tinnitus persistence, the neural networks underlying such alteration are unclear. The present study investigated the effect of tinnitus on emotional processing in middle-aged adults using functional magnetic resonance imaging and stimuli from the International Affective Digital Sounds database. There were three groups of participants: bilateral hearing loss with tinnitus (TIN), age- and gender-matched controls with bilateral hearing loss without tinnitus (HL) and matched normal hearing controls without tinnitus (NH). In the scanner, subjects rated sounds as pleasant, unpleasant, or neutral. The TIN and NH groups, but not the HL group, responded faster to affective sounds compared to neutral sounds. The TIN group had elevated response in bilateral parahippocampus and right insula compared to the NH group, and left parahippocampus compared to HL controls for pleasant relative to neutral sounds. A region-of-interest analysis detected increased activation for NH controls in the right amygdala when responding to affective stimuli, but failed to find a similar heightened response in the TIN and HL groups. All three groups showed increased response in auditory cortices for the affective relative to neutral sounds comparisons. Our results suggest that the emotional processing network is altered in tinnitus to rely on the parahippocampus and insula, rather than the amygdala, and this alteration may maintain a select advantage for the rapid processing of affective stimuli despite the hearing loss. The complex interaction of tinnitus and the limbic system should be accounted for in development of new tinnitus management strategies.

KW - Emotion

KW - IADS

KW - Tinnitus

KW - fMRI

UR - http://www.scopus.com/inward/record.url?scp=84901243423&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84901243423&partnerID=8YFLogxK

U2 - 10.1016/j.brainres.2014.04.024

DO - 10.1016/j.brainres.2014.04.024

M3 - Article

C2 - 24769166

AN - SCOPUS:84901243423

VL - 1567

SP - 28

EP - 41

JO - Brain Research

JF - Brain Research

SN - 0006-8993

ER -