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Effects of congruent and incongruent visual cues on speech perception and brain activity in cochlear implant users

Abstract

While deafness-induced plasticity has been investigated in the visual and auditory domains, not much is known about language processing in audiovisual multimodal environments for patients with restored hearing via cochlear implant (CI) devices. Here, we examined the effect of agreeing or conflicting visual inputs on auditory processing in deaf patients equipped with degraded artificial hearing. Ten post-lingually deafened CI users with good performance, along with matched control subjects, underwent H 2 15 O-positron emission tomography scans while carrying out a behavioral task requiring the extraction of speech information from unimodal auditory stimuli, bimodal audiovisual congruent stimuli, and incongruent stimuli. Regardless of congruency, the control subjects demonstrated activation of the auditory and visual sensory cortices, as well as the superior temporal sulcus, the classical multisensory integration area, indicating a bottom-up multisensory processing strategy. Compared to CI users, the control subjects exhibited activation of the right ventral premotor-supramarginal pathway. In contrast, CI users activated primarily the visual cortices more in the congruent audiovisual condition than in the null condition. In addition, compared to controls, CI users displayed an activation focus in the right amygdala for congruent audiovisual stimuli. The most notable difference between the two groups was an activation focus in the left inferior frontal gyrus in CI users confronted with incongruent audiovisual stimuli, suggesting top-down cognitive modulation for audiovisual conflict. Correlation analysis revealed that good speech performance was positively correlated with right amygdala activity for the congruent condition, but negatively correlated with bilateral visual cortices regardless of congruency. Taken together these results suggest that for multimodal inputs, cochlear implant users are more vision-reliant when processing congruent stimuli and are disturbed more by visual distractors when confronted with incongruent audiovisual stimuli. To cope with this multimodal conflict, CI users activate the left inferior frontal gyrus to adopt a top-down cognitive modulation pathway, whereas normal hearing individuals primarily adopt a bottom-up strategy.

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Abbreviations

NH:

Normal hearing

AV:

Audiovisual

STS:

Superior temporal sulcus

IFG:

Inferior frontal gyrus

CI:

Cochlear implant

PET:

Positron emission tomography

MRI:

Magnetic resonance imaging

CAP:

Categories of auditory performance

MTG:

Middle temporal gyrus

ITG:

Inferior temporal gyrus

rCBF:

Regional cerebral blood flow

vPMC:

Ventral premotor cortex

SMG:

Supramarginal gyrus

SFG:

Superior frontal gyrus

MeFG:

Medial frontal gyrus

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Acknowledgments

The authors thank Dr. Yong-Hwi Ahn for his support on the manuscript. Also, the first author thanks Dr. DY Yoon for giving precious support to the study. This work was supported by Korean government (MOST) [Korea Science and Engineering Foundation (KOSEF) (no. 2012-0030102)].

Author information

Correspondence to Seung Ha Oh.

Additional information

Jae-Jin Song and Hyo-Jeong Lee contributed equally to this work.

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Song, J., Lee, H., Kang, H. et al. Effects of congruent and incongruent visual cues on speech perception and brain activity in cochlear implant users. Brain Struct Funct 220, 1109–1125 (2015). https://doi.org/10.1007/s00429-013-0704-6

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Keywords

  • Cochlear implant
  • Deafness
  • Positron emission tomography
  • Audiovisual
  • Plasticity