The Visual Word Form Area compensates for auditory working memory dysfunction in schizophrenia

Alexander B. Herman; Ethan G. Brown; Corby L. Dale; Leighton B. Hinkley; Karuna Subramaniam; John F. Houde; Melissa Fisher; Sophia Vinogradov; Srikantan S. Nagarajan

doi:10.1038/s41598-020-63962-0

The Visual Word Form Area compensates for auditory working memory dysfunction in schizophrenia

Alexander B. Herman, Ethan G. Brown, Corby L. Dale, Leighton B. Hinkley, Karuna Subramaniam, John F. Houde, Melissa Fisher, Sophia Vinogradov, Srikantan S. Nagarajan

Psychiatry & Behavioral Sciences

Research output: Contribution to journal › Article › peer-review

3 Scopus citations

Abstract

Auditory working memory impairments feature prominently in schizophrenia. However, the existence of altered and perhaps compensatory neural dynamics, sub-serving auditory working memory, remains largely unexplored. We compared the dynamics of induced high gamma power (iHGP) across cortex in humans during speech-sound working memory in individuals with schizophrenia (SZ) and healthy comparison subjects (HC) using magnetoencephalography (MEG). SZ showed similar task performance to HC while utilizing different brain regions. During encoding of speech sounds, SZ lacked the correlation of iHGP with task performance in posterior superior temporal gyrus (STGp) that was observed in healthy subjects. Instead, SZ recruited the visual word form area (VWFA) during both stimulus encoding and response preparation. Importantly, VWFA activity during encoding correlated with the magnitude of SZ hallucinations, task performance and an independent measure of verbal working memory. These findings suggest that VWFA plasticity is harnessed to compensate for STGp dysfunction in schizophrenia patients with hallucinations.

Original language	English (US)
Article number	8881
Journal	Scientific reports
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41598-020-63962-0
State	Published - Jun 1 2020

Bibliographical note

Funding Information:
This work was funded in part by National Institutes of Health grants (R01DC004855, R01DC176960, R01DC010145, R01NS100440, R21NS076171, R01MH068725 and R01DC013979), UCOP MRIP MRP-17– 454755, National Science Foundation grant (BCS 1262297), the Howard Hughes Medical Institute Research Fellowship Program, the US Department of Defense grant (W81XWH-13-1-0494) and the San Francisco Department of Veterans’ Affairs Medical Center.

Publisher Copyright:
© 2020, The Author(s).

Keywords

Adult
Case-Control Studies
Female
Humans
Magnetoencephalography
Male
Memory Disorders/diagnosis
Memory, Short-Term/physiology
Middle Aged
Phonetics
Prefrontal Cortex/physiopathology
Schizophrenia/physiopathology
Schizophrenic Psychology
Speech Perception
Temporal Lobe/physiopathology
Young Adult

PubMed: MeSH publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Randomized Controlled Trial
Journal Article
Research Support, N.I.H., Extramural

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title = "The Visual Word Form Area compensates for auditory working memory dysfunction in schizophrenia",

abstract = "Auditory working memory impairments feature prominently in schizophrenia. However, the existence of altered and perhaps compensatory neural dynamics, sub-serving auditory working memory, remains largely unexplored. We compared the dynamics of induced high gamma power (iHGP) across cortex in humans during speech-sound working memory in individuals with schizophrenia (SZ) and healthy comparison subjects (HC) using magnetoencephalography (MEG). SZ showed similar task performance to HC while utilizing different brain regions. During encoding of speech sounds, SZ lacked the correlation of iHGP with task performance in posterior superior temporal gyrus (STGp) that was observed in healthy subjects. Instead, SZ recruited the visual word form area (VWFA) during both stimulus encoding and response preparation. Importantly, VWFA activity during encoding correlated with the magnitude of SZ hallucinations, task performance and an independent measure of verbal working memory. These findings suggest that VWFA plasticity is harnessed to compensate for STGp dysfunction in schizophrenia patients with hallucinations.",

keywords = "Adult, Case-Control Studies, Female, Humans, Magnetoencephalography, Male, Memory Disorders/diagnosis, Memory, Short-Term/physiology, Middle Aged, Phonetics, Prefrontal Cortex/physiopathology, Schizophrenia/physiopathology, Schizophrenic Psychology, Speech Perception, Temporal Lobe/physiopathology, Young Adult",

author = "Herman, {Alexander B.} and Brown, {Ethan G.} and Dale, {Corby L.} and Hinkley, {Leighton B.} and Karuna Subramaniam and Houde, {John F.} and Melissa Fisher and Sophia Vinogradov and Nagarajan, {Srikantan S.}",

note = "Funding Information: This work was funded in part by National Institutes of Health grants (R01DC004855, R01DC176960, R01DC010145, R01NS100440, R21NS076171, R01MH068725 and R01DC013979), UCOP MRIP MRP-17– 454755, National Science Foundation grant (BCS 1262297), the Howard Hughes Medical Institute Research Fellowship Program, the US Department of Defense grant (W81XWH-13-1-0494) and the San Francisco Department of Veterans{\textquoteright} Affairs Medical Center. Publisher Copyright: {\textcopyright} 2020, The Author(s).",

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doi = "10.1038/s41598-020-63962-0",

language = "English (US)",

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AU - Herman, Alexander B.

AU - Brown, Ethan G.

AU - Dale, Corby L.

AU - Hinkley, Leighton B.

AU - Subramaniam, Karuna

AU - Houde, John F.

AU - Fisher, Melissa

AU - Vinogradov, Sophia

AU - Nagarajan, Srikantan S.

N1 - Funding Information: This work was funded in part by National Institutes of Health grants (R01DC004855, R01DC176960, R01DC010145, R01NS100440, R21NS076171, R01MH068725 and R01DC013979), UCOP MRIP MRP-17– 454755, National Science Foundation grant (BCS 1262297), the Howard Hughes Medical Institute Research Fellowship Program, the US Department of Defense grant (W81XWH-13-1-0494) and the San Francisco Department of Veterans’ Affairs Medical Center. Publisher Copyright: © 2020, The Author(s).

PY - 2020/6/1

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N2 - Auditory working memory impairments feature prominently in schizophrenia. However, the existence of altered and perhaps compensatory neural dynamics, sub-serving auditory working memory, remains largely unexplored. We compared the dynamics of induced high gamma power (iHGP) across cortex in humans during speech-sound working memory in individuals with schizophrenia (SZ) and healthy comparison subjects (HC) using magnetoencephalography (MEG). SZ showed similar task performance to HC while utilizing different brain regions. During encoding of speech sounds, SZ lacked the correlation of iHGP with task performance in posterior superior temporal gyrus (STGp) that was observed in healthy subjects. Instead, SZ recruited the visual word form area (VWFA) during both stimulus encoding and response preparation. Importantly, VWFA activity during encoding correlated with the magnitude of SZ hallucinations, task performance and an independent measure of verbal working memory. These findings suggest that VWFA plasticity is harnessed to compensate for STGp dysfunction in schizophrenia patients with hallucinations.

AB - Auditory working memory impairments feature prominently in schizophrenia. However, the existence of altered and perhaps compensatory neural dynamics, sub-serving auditory working memory, remains largely unexplored. We compared the dynamics of induced high gamma power (iHGP) across cortex in humans during speech-sound working memory in individuals with schizophrenia (SZ) and healthy comparison subjects (HC) using magnetoencephalography (MEG). SZ showed similar task performance to HC while utilizing different brain regions. During encoding of speech sounds, SZ lacked the correlation of iHGP with task performance in posterior superior temporal gyrus (STGp) that was observed in healthy subjects. Instead, SZ recruited the visual word form area (VWFA) during both stimulus encoding and response preparation. Importantly, VWFA activity during encoding correlated with the magnitude of SZ hallucinations, task performance and an independent measure of verbal working memory. These findings suggest that VWFA plasticity is harnessed to compensate for STGp dysfunction in schizophrenia patients with hallucinations.

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SN - 2045-2322

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JF - Scientific Reports

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ER -

The Visual Word Form Area compensates for auditory working memory dysfunction in schizophrenia

Abstract

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Keywords

PubMed: MeSH publication types

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