Convergence of semantics and emotional expression within the IFG pars orbitalis

Michel Belyk, Steven Brown, Jessica Lim, Sonja A. Kotz

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Humans communicate through a combination of linguistic and emotional channels, including propositional speech, writing, sign language, music, but also prosodic, facial, and gestural expression. These channels can be interpreted separately or they can be integrated to multimodally convey complex meanings. Neural models of the perception of semantics and emotion include nodes for both functions in the inferior frontal gyrus pars orbitalis (IFGorb). However, it is not known whether this convergence involves a common functional zone or instead specialized subregions that process semantics and emotion separately. To address this, we performed Kernel Density Estimation meta-analyses of published neuroimaging studies of the perception of semantics or emotion that reported activation in the IFGorb. The results demonstrated that the IFGorb contains two zones with distinct functional profiles. A lateral zone, situated immediately ventral to Broca's area, was implicated in both semantics and emotion. Another zone, deep within the ventral frontal operculum, was engaged almost exclusively by studies of emotion. Follow-up analysis using Meta-Analytic Connectivity Modeling demonstrated that both zones were frequently co-activated with a common network of sensory, motor, and limbic structures, although the lateral zone had a greater association with prefrontal cortical areas involved in executive function. The status of the lateral IFGorb as a point of convergence between the networks for processing semantic and emotional content across modalities of communication is intriguing since this structure is preserved across primates with limited semantic abilities. Hence, the IFGorb may have initially evolved to support the comprehension of emotional signals, being later co-opted to support semantic communication in humans by forming new connections with brain regions that formed the human semantic network.

Original languageEnglish
Pages (from-to)240-248
Number of pages9
JournalNeuroimage
Volume156
DOIs
Publication statusPublished - Aug 2017

Keywords

  • Inferior frontal gyrus
  • Pars orbitalis
  • Emotion
  • Semantics
  • Meta-analysis
  • Parcellation
  • LIKELIHOOD ESTIMATION METAANALYSIS
  • MONKEY FRONTAL-CORTEX
  • RIGHT-HEMISPHERE
  • PREFRONTAL CORTEX
  • COGNITIVE CONTROL
  • AFFECTIVE PROSODY
  • ALE METAANALYSIS
  • HUMAN BRAIN
  • LANGUAGE
  • ACTIVATION

Cite this

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title = "Convergence of semantics and emotional expression within the IFG pars orbitalis",
abstract = "Humans communicate through a combination of linguistic and emotional channels, including propositional speech, writing, sign language, music, but also prosodic, facial, and gestural expression. These channels can be interpreted separately or they can be integrated to multimodally convey complex meanings. Neural models of the perception of semantics and emotion include nodes for both functions in the inferior frontal gyrus pars orbitalis (IFGorb). However, it is not known whether this convergence involves a common functional zone or instead specialized subregions that process semantics and emotion separately. To address this, we performed Kernel Density Estimation meta-analyses of published neuroimaging studies of the perception of semantics or emotion that reported activation in the IFGorb. The results demonstrated that the IFGorb contains two zones with distinct functional profiles. A lateral zone, situated immediately ventral to Broca's area, was implicated in both semantics and emotion. Another zone, deep within the ventral frontal operculum, was engaged almost exclusively by studies of emotion. Follow-up analysis using Meta-Analytic Connectivity Modeling demonstrated that both zones were frequently co-activated with a common network of sensory, motor, and limbic structures, although the lateral zone had a greater association with prefrontal cortical areas involved in executive function. The status of the lateral IFGorb as a point of convergence between the networks for processing semantic and emotional content across modalities of communication is intriguing since this structure is preserved across primates with limited semantic abilities. Hence, the IFGorb may have initially evolved to support the comprehension of emotional signals, being later co-opted to support semantic communication in humans by forming new connections with brain regions that formed the human semantic network.",
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author = "Michel Belyk and Steven Brown and Jessica Lim and Kotz, {Sonja A.}",
note = "Copyright {\circledC} 2017 Elsevier Inc. All rights reserved.",
year = "2017",
month = "8",
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language = "English",
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Convergence of semantics and emotional expression within the IFG pars orbitalis. / Belyk, Michel; Brown, Steven; Lim, Jessica; Kotz, Sonja A.

In: Neuroimage, Vol. 156, 08.2017, p. 240-248.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Convergence of semantics and emotional expression within the IFG pars orbitalis

AU - Belyk, Michel

AU - Brown, Steven

AU - Lim, Jessica

AU - Kotz, Sonja A.

N1 - Copyright © 2017 Elsevier Inc. All rights reserved.

PY - 2017/8

Y1 - 2017/8

N2 - Humans communicate through a combination of linguistic and emotional channels, including propositional speech, writing, sign language, music, but also prosodic, facial, and gestural expression. These channels can be interpreted separately or they can be integrated to multimodally convey complex meanings. Neural models of the perception of semantics and emotion include nodes for both functions in the inferior frontal gyrus pars orbitalis (IFGorb). However, it is not known whether this convergence involves a common functional zone or instead specialized subregions that process semantics and emotion separately. To address this, we performed Kernel Density Estimation meta-analyses of published neuroimaging studies of the perception of semantics or emotion that reported activation in the IFGorb. The results demonstrated that the IFGorb contains two zones with distinct functional profiles. A lateral zone, situated immediately ventral to Broca's area, was implicated in both semantics and emotion. Another zone, deep within the ventral frontal operculum, was engaged almost exclusively by studies of emotion. Follow-up analysis using Meta-Analytic Connectivity Modeling demonstrated that both zones were frequently co-activated with a common network of sensory, motor, and limbic structures, although the lateral zone had a greater association with prefrontal cortical areas involved in executive function. The status of the lateral IFGorb as a point of convergence between the networks for processing semantic and emotional content across modalities of communication is intriguing since this structure is preserved across primates with limited semantic abilities. Hence, the IFGorb may have initially evolved to support the comprehension of emotional signals, being later co-opted to support semantic communication in humans by forming new connections with brain regions that formed the human semantic network.

AB - Humans communicate through a combination of linguistic and emotional channels, including propositional speech, writing, sign language, music, but also prosodic, facial, and gestural expression. These channels can be interpreted separately or they can be integrated to multimodally convey complex meanings. Neural models of the perception of semantics and emotion include nodes for both functions in the inferior frontal gyrus pars orbitalis (IFGorb). However, it is not known whether this convergence involves a common functional zone or instead specialized subregions that process semantics and emotion separately. To address this, we performed Kernel Density Estimation meta-analyses of published neuroimaging studies of the perception of semantics or emotion that reported activation in the IFGorb. The results demonstrated that the IFGorb contains two zones with distinct functional profiles. A lateral zone, situated immediately ventral to Broca's area, was implicated in both semantics and emotion. Another zone, deep within the ventral frontal operculum, was engaged almost exclusively by studies of emotion. Follow-up analysis using Meta-Analytic Connectivity Modeling demonstrated that both zones were frequently co-activated with a common network of sensory, motor, and limbic structures, although the lateral zone had a greater association with prefrontal cortical areas involved in executive function. The status of the lateral IFGorb as a point of convergence between the networks for processing semantic and emotional content across modalities of communication is intriguing since this structure is preserved across primates with limited semantic abilities. Hence, the IFGorb may have initially evolved to support the comprehension of emotional signals, being later co-opted to support semantic communication in humans by forming new connections with brain regions that formed the human semantic network.

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KW - Meta-analysis

KW - Parcellation

KW - LIKELIHOOD ESTIMATION METAANALYSIS

KW - MONKEY FRONTAL-CORTEX

KW - RIGHT-HEMISPHERE

KW - PREFRONTAL CORTEX

KW - COGNITIVE CONTROL

KW - AFFECTIVE PROSODY

KW - ALE METAANALYSIS

KW - HUMAN BRAIN

KW - LANGUAGE

KW - ACTIVATION

U2 - 10.1016/j.neuroimage.2017.04.020

DO - 10.1016/j.neuroimage.2017.04.020

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VL - 156

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EP - 248

JO - Neuroimage

JF - Neuroimage

SN - 1053-8119

ER -