Emotional facial expression and perioral motor functions of the human auditory cortex

Ravindra Arya; Brian Ervin; Hansel M Greiner; Jason Buroker; Anna W Byars; Jeffrey R Tenney; Todd M Arthur; Susan L Fong; Nan Lin; Clayton Frink; Leonid Rozhkov; Craig Scholle; Jesse Skoch; James L Leach; Francesco T Mangano; Tracy A Glauser; Gregory Hickok; Katherine D Holland

doi:10.1016/j.clinph.2024.04.017

Emotional facial expression and perioral motor functions of the human auditory cortex

Clin Neurophysiol. 2024 Apr 30:163:102-111. doi: 10.1016/j.clinph.2024.04.017. Online ahead of print.

Authors

Ravindra Arya¹, Brian Ervin², Hansel M Greiner³, Jason Buroker⁴, Anna W Byars³, Jeffrey R Tenney³, Todd M Arthur³, Susan L Fong³, Nan Lin³, Clayton Frink⁴, Leonid Rozhkov⁴, Craig Scholle⁴, Jesse Skoch⁵, James L Leach⁶, Francesco T Mangano⁵, Tracy A Glauser³, Gregory Hickok⁷, Katherine D Holland³

Affiliations

¹ Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH, USA; Department of Electrical Engineering and Computer Science, University of Cincinnati, Cincinnati, OH, USA. Electronic address: Ravindra.Arya@cchmc.org.
² Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA; Department of Electrical Engineering and Computer Science, University of Cincinnati, Cincinnati, OH, USA.
³ Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH, USA.
⁴ Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
⁵ Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH, USA; Division of Pediatric Neurosurgery, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
⁶ Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH, USA; Division of Pediatric Neuro-radiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
⁷ Department of Cognitive Sciences, Department of Language Science, University of California, Irvine, CA, USA.

PMID: 38729074
DOI: 10.1016/j.clinph.2024.04.017

Abstract

Objective: We investigated the role of transverse temporal gyrus and adjacent cortex (TTG+) in facial expressions and perioral movements.

Methods: In 31 patients undergoing stereo-electroencephalography monitoring, we describe behavioral responses elicited by electrical stimulation within the TTG+. Task-induced high-gamma modulation (HGM), auditory evoked responses, and resting-state connectivity were used to investigate the cortical sites having different types of responses on electrical stimulation.

Results: Changes in facial expressions and perioral movements were elicited on electrical stimulation within TTG+ in 9 (29%) and 10 (32%) patients, respectively, in addition to the more common language responses (naming interruptions, auditory hallucinations, paraphasic errors). All functional sites showed auditory task induced HGM and evoked responses validating their location within the auditory cortex, however, motor sites showed lower peak amplitudes and longer peak latencies compared to language sites. Significant first-degree connections for motor sites included precentral, anterior cingulate, parahippocampal, and anterior insular gyri, whereas those for language sites included posterior superior temporal, posterior middle temporal, inferior frontal, supramarginal, and angular gyri.

Conclusions: Multimodal data suggests that TTG+ may participate in auditory-motor integration.

Significance: TTG+ likely participates in facial expressions in response to emotional cues during an auditory discourse.

Keywords: Drug-resistant epilepsy; Functional brain mapping; Heschl's gyrus; High-gamma modulation; Stereo EEG; Transverse temporal gyrus.