The Neural Processing of Vocal Emotion After Hearing Reconstruction in Prelingual Deaf Children: A Functional Near-Infrared Spectroscopy Brain Imaging Study.

Yuyang Wang,Lili Liu,Qiang He,Chaogang Wei,Ying Zhang,Tianyu Xin,Xinlin Hou,Yuhe Liu

doi:10.3389/fnins.2021.705741

Abstract

As elucidated by prior research, children with hearing loss have impaired vocal emotion recognition compared with their normal-hearing peers. Cochlear implants (CIs) have achieved significant success in facilitating hearing and speech abilities for people with severe-to-profound sensorineural hearing loss. However, due to the current limitations in neuroimaging tools, existing research has been unable to detail the neural processing for perception and the recognition of vocal emotions during early stage CI use in infant and toddler CI users (ITCI). In the present study, functional near-infrared spectroscopy (fNIRS) imaging was employed during preoperative and postoperative tests to describe the early neural processing of perception in prelingual deaf ITCIs and their recognition of four vocal emotions (fear, anger, happiness, and neutral). The results revealed that the cortical response elicited by vocal emotional stimulation on the left pre-motor and supplementary motor area (pre-SMA), right middle temporal gyrus (MTG), and right superior temporal gyrus (STG) were significantly different between preoperative and postoperative tests. These findings indicate differences between the preoperative and postoperative neural processing associated with vocal emotional stimulation. Further results revealed that the recognition of vocal emotional stimuli appeared in the right supramarginal gyrus (SMG) after CI implantation, and the response elicited by fear was significantly greater than the response elicited by anger, indicating a negative bias. These findings indicate that the development of emotional bias and the development of emotional perception and recognition capabilities in ITCIs occur on a different timeline and involve different neural processing from those in normal-hearing peers. To assess the speech perception and production abilities, the Infant-Toddler Meaningful Auditory Integration Scale (IT-MAIS) and Speech Intelligibility Rating (SIR) were used. The results revealed no significant differences between preoperative and postoperative tests. Finally, the correlates of the neurobehavioral results were investigated, and the results demonstrated that the preoperative response of the right SMG to anger stimuli was significantly and positively correlated with the evaluation of postoperative behavioral outcomes. And the postoperative response of the right SMG to anger stimuli was significantly and negatively correlated with the evaluation of postoperative behavioral outcomes.

Highlights

Emotional communication is a universal form of expression that enables people to overcome language and cultural barriers (Thompson and Balkwill, 2006; Bryant and Barrett, 2008; Pell et al, 2009)
The results showed that vocal emotions enhance the activation of the right superior temporal gyrus (STG), the left superior frontal gyrus (SFG), and the left angular gyrus, which may indicate the regions associated with the neural processing of vocal emotional perception during neonatal development
Participants met the following criteria: (A) except for hearing, other physiological development was normal; (B) imaging examinations showed no deformities of the inner ear; (C) the postoperative X-ray examination did not reveal any abnormalities, and implanted electrodes were correctly located in the cochlea; (D) all impedances for all electrodes after surgery are within the normal range; (E) the clinical team evaluated the comfort and threshold levels of each electrode position according to standard clinical protocols; and (F) the participants were clinically asymptomatic (No abnormality or discomfort) at the two times of functional near-infrared spectroscopy (fNIRS) recording

Summary

Introduction

Emotional communication is a universal form of expression that enables people to overcome language and cultural barriers (Thompson and Balkwill, 2006; Bryant and Barrett, 2008; Pell et al, 2009). In other research, newborns have been shown to have a preference for the infant-directed speech of female voices, which can be attributed to infant-directed speech generally conveying more emotion and information, compared with the suppressed emotion expression in most adult communication (Glenn and Cunningham, 1983; Cooper and Aslin, 1989; Pegg et al, 1992). These findings revealed that the perception and recognition of vocal emotions are significant factors during cognition and communication in early life. Infants and toddlers with hearing loss face difficulties in emotional communications (Ludlow et al, 2010; Most and Michaelis, 2012)

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