Abstract
Alzheimer’s disease (AD) is a neurodegenerative disease involving cognitive impairment and abnormalities in speech and language. Here, we examine how AD affects the fidelity of auditory feedback predictions during speaking. We focus on the phenomenon of speaking-induced suppression (SIS), the auditory cortical responses’ suppression during auditory feedback processing. SIS is determined by subtracting the magnitude of auditory cortical responses during speaking from listening to playback of the same speech. Our state feedback control model of speech motor control explains SIS as arising from the onset of auditory feedback matching a prediction of that feedback onset during speaking – a prediction that is absent during passive listening to playback of the auditory feedback. Our model hypothesizes that the auditory cortical response to auditory feedback reflects the mismatch with the prediction: small during speaking, large during listening, with the difference being SIS. Normally, during speaking, auditory feedback matches its predictions, then SIS will be large. Any reductions in SIS will indicate inaccuracy in auditory feedback prediction not matching the actual feedback. We investigated SIS in AD patients (n = 20; mean (SD) age, 60.77 (10.04); female (%), 55.00) and healthy controls (n = 12; mean (SD) age, 63.68 (6.07); female (%), 83.33) through magnetoencephalography-based functional imaging. We found a significant reduction in SIS at approximately 100 ms in AD patients compared to healthy controls (linear mixed effects model, F(1, 57.5) = 6.849, p = 0.011). The results suggest that AD patients generate inaccurate auditory feedback predictions, contributing to abnormalities in AD speech.
Significance statement
Speaking-induced suppression (SIS) refers to the suppressed response to auditory feedback heard during speaking, compared to the response to the same feedback heard during passive listening. We posit that SIS arises from a comparison between auditory feedback and a motor-efference-copy-derived feedback prediction. During speaking, feedback matches prediction, resulting in small auditory responses. Passive listening to playback of this feedback matches no prediction, resulting in large auditory responses. Thus, SIS measures the accuracy of feedback predictions. The absence of SIS that we found in AD patients suggests they have impaired feedback predictions, which may be indicative of a more widespread impairment in generating predictions that may be manifested in the earliest stages of AD progression.
- speaking-induced suppression
- Alzheimer’s disease
- state feedback control model
- efference copy
- magnetoencephalography
Footnotes
The authors declare no competing financial interests.
This study was funded by the National Institutes of Health grants: R01DC017696 (J.F.H., S.S.N.), 3R01DC017696-01S1 (J.F.H., S.S.N.), R01DC017091 (J.F.H., S.S.N.), R01DC010145 (J.F.H.), R21NS076171 (S.S.N.), R01NS100440 (J.F.H., S.S.N., M.L.G.-T.), R01EB022717 (S.S.N.), F32AG050434-01A1 (K.G.R.), K08AG058749 (K.G.R.), and K23AG038357 (K.V.); National Science Foundation Grant BCS-1262297 (S.S.N.); a grant from John Douglas French Alzheimer’s Foundation (K.V.); a grant from Larry L. Hillblom Foundation, 2015-A-034-FEL (K.G.R); University of California San Francisco Alzheimer’s Disease Research Center pilot project grant (K.V); grants from the Alzheimer’s Association, and made possible by Part the Cloud: PCTRB-13-288476 (K.V.), and ETAC-09-133596 (J.F.H.); a gift from Ricoh Inc. (S.S.N.); and a gift from the S.D. Bechtel Jr. Foundation (K.V.). The authors thank all participants and their families for supporting this research.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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