Aberrant Modulation of Broadband Neural Oscillations Reflects Vocal Sensorimotor Deficits in Post-stroke Aphasia

Overview

Journal Clin Neurophysiol

Publisher Elsevier

Specialties Neurology
Psychiatry

Date 2023 Mar 19

PMID 36934601

Authors

Roozbeh Behroozmand

Kimaya Sarmukadam

Julius Fridriksson

Affiliations

Soon will be listed here.

Abstract

Objective: The present study investigated the neural oscillatory correlates of impaired vocal sensorimotor control in left-hemisphere stroke.

Methods: Electroencephalography (EEG) signals were recorded from 34 stroke and 46 control subjects during speech vowel vocalization and listening tasks under normal and pitch-shifted auditory feedback.

Results: Time-frequency analyses revealed aberrantly decreased theta (4-8 Hz) and increased gamma band (30-80 Hz) power in frontal and posterior parieto-occipital regions as well as reduced alpha (8-13 Hz) and beta (13-30 Hz) desynchronization over sensorimotor areas before speech vowel vocalization in left-hemisphere stroke compared with controls. Subjects with the stroke also presented with aberrant modulation of broadband (4-80 Hz) neural oscillations over sensorimotor regions after speech vowel onset during vocalization and listening under normal and altered auditory feedback. We found that the atypical pattern of broadband neural oscillatory modulation was correlated with diminished vocal feedback error compensation behavior and the severity of co-existing language-related aphasia symptoms associated with left-hemisphere stroke.

Conclusions: These findings indicate complex interplays between the underlying mechanisms of speech and language and their deficits in post-stroke aphasia.

Significance: Our data motivate the notion of studying neural oscillatory dynamics as a critical component for the examination of speech and language disorders in post-stroke aphasia.

Citing Articles

Neural oscillations reveal disrupted functional connectivity associated with impaired speech auditory feedback control in post-stroke aphasia.

Sarmukadam K, Behroozmand R Cortex. 2023; 166:258-274.

PMID: 37437320 PMC: 10527672. DOI: 10.1016/j.cortex.2023.05.015.

References

Sengupta R, Nasir S . The predictive roles of neural oscillations in speech motor adaptability. J Neurophysiol. 2016; 115(5):2519-28. PMC: 4922470. DOI: 10.1152/jn.00043.2016. View

Wilmskoetter J, Del Gaizo J, Phillip L, Behroozmand R, Gleichgerrcht E, Fridriksson J . Predicting naming responses based on pre-articulatory electrical activity in individuals with aphasia. Clin Neurophysiol. 2019; 130(11):2153-2163. PMC: 6935719. DOI: 10.1016/j.clinph.2019.08.011. View

Yourganov G, Stark B, Fridriksson J, Bonilha L, Rorden C . Effect of Stroke on Contralateral Functional Connectivity. Brain Connect. 2021; 11(7):543-552. PMC: 8558087. DOI: 10.1089/brain.2020.0901. View

Hari R, Forss N, Avikainen S, Kirveskari E, Salenius S, Rizzolatti G . Activation of human primary motor cortex during action observation: a neuromagnetic study. Proc Natl Acad Sci U S A. 1998; 95(25):15061-5. PMC: 24575. DOI: 10.1073/pnas.95.25.15061. View

Hickok G . The cortical organization of speech processing: feedback control and predictive coding the context of a dual-stream model. J Commun Disord. 2012; 45(6):393-402. PMC: 3468690. DOI: 10.1016/j.jcomdis.2012.06.004. View

Hari R, Salmelin R . Human cortical oscillations: a neuromagnetic view through the skull. Trends Neurosci. 1997; 20(1):44-9. DOI: 10.1016/S0166-2236(96)10065-5. View

Oztop E, Kawato M, Arbib M . Mirror neurons: functions, mechanisms and models. Neurosci Lett. 2012; 540:43-55. DOI: 10.1016/j.neulet.2012.10.005. View

Poeppel D, Assaneo M . Speech rhythms and their neural foundations. Nat Rev Neurosci. 2020; 21(6):322-334. DOI: 10.1038/s41583-020-0304-4. View

Behroozmand R, Phillip L, Johari K, Bonilha L, Rorden C, Hickok G . Sensorimotor impairment of speech auditory feedback processing in aphasia. Neuroimage. 2017; 165:102-111. PMC: 5732035. DOI: 10.1016/j.neuroimage.2017.10.014. View

10.

Canolty R, Edwards E, Dalal S, Soltani M, Nagarajan S, Kirsch H . High gamma power is phase-locked to theta oscillations in human neocortex. Science. 2006; 313(5793):1626-8. PMC: 2628289. DOI: 10.1126/science.1128115. View

11.

Johari K, Behroozmand R . Neural correlates of speech and limb motor timing deficits revealed by aberrant beta band desynchronization in Parkinson's disease. Clin Neurophysiol. 2021; 132(10):2711-2721. DOI: 10.1016/j.clinph.2021.06.022. View

12.

Howard M, Poeppel D . Discrimination of speech stimuli based on neuronal response phase patterns depends on acoustics but not comprehension. J Neurophysiol. 2010; 104(5):2500-11. PMC: 2997028. DOI: 10.1152/jn.00251.2010. View

13.

Fridriksson J, Yourganov G, Bonilha L, Basilakos A, den Ouden D, Rorden C . Revealing the dual streams of speech processing. Proc Natl Acad Sci U S A. 2016; 113(52):15108-15113. PMC: 5206517. DOI: 10.1073/pnas.1614038114. View

14.

Tzagarakis C, Ince N, Leuthold A, Pellizzer G . Beta-band activity during motor planning reflects response uncertainty. J Neurosci. 2010; 30(34):11270-7. PMC: 6633326. DOI: 10.1523/JNEUROSCI.6026-09.2010. View

15.

Giraud A, Poeppel D . Cortical oscillations and speech processing: emerging computational principles and operations. Nat Neurosci. 2012; 15(4):511-7. PMC: 4461038. DOI: 10.1038/nn.3063. View

16.

Johnson L, Sangtian S, Johari K, Behroozmand R, Fridriksson J . Slowed Compensation Responses to Altered Auditory Feedback in Post-Stroke Aphasia: Implications for Speech Sensorimotor Integration. J Commun Disord. 2020; 88:106034. PMC: 7736368. DOI: 10.1016/j.jcomdis.2020.106034. View

17.

Houde J, Nagarajan S . Speech production as state feedback control. Front Hum Neurosci. 2011; 5:82. PMC: 3200525. DOI: 10.3389/fnhum.2011.00082. View

18.

Jenson D, Bowers A, Harkrider A, Thornton D, Cuellar M, Saltuklaroglu T . Temporal dynamics of sensorimotor integration in speech perception and production: independent component analysis of EEG data. Front Psychol. 2014; 5:656. PMC: 4091311. DOI: 10.3389/fpsyg.2014.00656. View

19.

Thibaut A, Simis M, Battistella L, Fanciullacci C, Bertolucci F, Huerta-Gutierrez R . Using Brain Oscillations and Corticospinal Excitability to Understand and Predict Post-Stroke Motor Function. Front Neurol. 2017; 8:187. PMC: 5423894. DOI: 10.3389/fneur.2017.00187. View

20.

Buzsaki G, Draguhn A . Neuronal oscillations in cortical networks. Science. 2004; 304(5679):1926-9. DOI: 10.1126/science.1099745. View