Neuroplasticity of language in left-hemisphere stroke: evidence linking subsecond electrophysiology and structural connectivity
-
1
University of California Berkeley, United States
-
2
Veterans Affairs Northern California Health Care System, Center for Aphasia and Related Disorders, United States
-
3
Max Planck Institute for Human Cognitive and Brain Sciences, Department of Neuropsychology, Germany
-
4
University of California Davis, Department of Neurology, United States
Language function is often impaired following stroke to the left hemisphere, compromising quality of everyday life. Our current understanding of functional compensation is predominantly based on haemodynamic brain measures. With these measures, functional compensation by the unaffected right hemisphere has been observed in language recovery. Yet, language processing occurs in the subsecond time scale and language neuroplasticity must also be addressed by electrophysiological measures that track the time course of language function. We combined for the first time behavioral, electrophysiological, and structural-connectivity measures to characterize neuroplasticity underlying successful compensation of language abilities after left-hemispheric stroke. We recorded the electroencephalogram from six patients with stroke lesions to the left temporal lobe and matched controls during context-driven word retrieval, a key aspect of language production. Participants heard context sentences that either constrained the final word (“He locked the door with the [key]”) or not (“She walked in here with the [key]”). The last word was shown as a picture that participants had to name. We conducted individual-participant analyses. For the EEG, we focused on oscillatory power as a subsecond indicator of a brain region's functional neurophysiological computations. We also investigated the relationship between white-matter integrity and hemispheric lateralization using the patients’ white-matter disconnection maps. Behaviorally, participants named pictures faster following constrained relative to unconstrained contexts. This effect was robust in all (ps < .001) but two patients (ps > .086), who had extensive damage to the left temporal and inferior parietal lobes. For the EEG, replicating prior findings, left-lateralized alpha-beta oscillatory power decreased in controls prior to picture presentation for constrained relative to unconstrained contexts (p < .001). In the patient group, the alpha-beta power decreases had the same time course and spectrum as in controls, but showed a striking lateralization to the intact right hemisphere (p < .001). Individual source localization analyses confirmed that the alpha-beta power decreases were predominantly right-lateralized in three patients. Given that posterior callosal fibers (i.e., splenium) directly connect left and right temporal lobes, we examined the relationship between hemispheric lateralization and splenium integrity. The patients’ hemispheric lateralization depended on the integrity of the splenium (Spearman’s rho = .942, p = .017). Finally, electrophysiological compensation enabled the behavioral compensation of language production, as only the patients without alpha-beta power decreases performed poorly behaviorally (p = .033). We provide novel evidence that intact interhemispheric white-matter connections enable the right hemisphere to compensate for impaired left-hemispheric language functions through similar neurophysiological computations. Our findings suggest that incorporating well-understood direct measures of neural activity into investigations of neuroplasticity can provide important neural markers to help predict language recovery, assess the progress of neurorehabilitation, and delineate targets for therapeutic neuromodulation.
Keywords:
Splenium,
EEG,
oscillations,
Aphasia,
Recovery,
Temporal Lobe
Conference:
54th Annual Academy of Aphasia Meeting, Llandudno, United Kingdom, 16 Oct - 18 Oct, 2016.
Presentation Type:
Platform Sessions
Topic:
Academy of Aphasia
Citation:
Piai
V,
Meyer
L,
Dronkers
NF and
Knight
RT
(2016). Neuroplasticity of language in left-hemisphere stroke: evidence linking subsecond electrophysiology and structural connectivity.
Front. Psychol.
Conference Abstract:
54th Annual Academy of Aphasia Meeting.
doi: 10.3389/conf.fpsyg.2016.68.00020
Copyright:
The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers.
They are made available through the Frontiers publishing platform as a service to conference organizers and presenters.
The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated.
Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed.
For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions.
Received:
19 Apr 2016;
Published Online:
15 Aug 2016.
*
Correspondence:
Dr. Vitória Piai, University of California Berkeley, Berkeley, United States, v.piai@donders.ru.nl