Convergence of semantics and emotional expression within the IFG pars orbitalis

• Published in: NeuroImage (Orlando, Fla.) Vol. 156; pp. 240 - 248
• Main Authors: Belyk, Michel, Brown, Steven, Lim, Jessica, Kotz, Sonja A.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01-08-2017; Elsevier Limited
• Subjects: Activation analysis; Brain; Brain research; Broca Area - anatomy & histology; Broca Area - physiology; Broca's area; Communication; Convergence; Cortex; Emotion; Emotions; Emotions - physiology; Executive function; Experiments; Frontal gyrus; Frontal lobe; Human communication; Humans; Inferior frontal gyrus; Information processing; Language; Magnetic Resonance Imaging; Mars; Medical imaging; Meta-analysis; Motor task performance; Neural networks; Neural Pathways - anatomy & histology; Neural Pathways - physiology; Neuroimaging; Neurology; Nodes; Operculum; Parcellation; Pars orbitalis; Perception; Primates; Semantics; Speech; Speech perception; Speech Perception - physiology; Emotion; Semantics; Parcellation; Inferior frontal gyrus; Pars orbitalis; Meta-analysis
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2017.04.020

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.
[Display omitted]
•The inferior frontal gyrus pars orbitalis (IFGorb) contains two separate functional zones•The lateral IFGorb is a zone of convergence for semantics and emotional expression•The lateral IFGorb has functional connectivity with both limbic and language areas•The opercular IFGorb is specialized for perceiving expressions of emotion•The opercular IFGorb has functional connectivity with the limbic system