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Research Articles, Behavioral/Cognitive

Simulated Attack Reveals How Lesions Affect Network Properties in Poststroke Aphasia

John D. Medaglia, Brian A. Erickson, Dorian Pustina, Apoorva S. Kelkar, Andrew T. DeMarco, J. Vivian Dickens and Peter E. Turkeltaub
Journal of Neuroscience 15 June 2022, 42 (24) 4913-4926; DOI: https://doi.org/10.1523/JNEUROSCI.1163-21.2022
John D. Medaglia
1Department of Psychology, Drexel University, Philadelphia, Pennsylvania 19104
2Department of Neurology, Drexel University, Philadelphia, Pennsylvania 19104
3Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104
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Brian A. Erickson
1Department of Psychology, Drexel University, Philadelphia, Pennsylvania 19104
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Dorian Pustina
4Cure Huntingdon's Disease Initiative (CHDI) Foundation, Princeton, New Jersey 08540
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Apoorva S. Kelkar
1Department of Psychology, Drexel University, Philadelphia, Pennsylvania 19104
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Andrew T. DeMarco
5Department of Neurology, Georgetown University, Washington, DC 20007
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J. Vivian Dickens
5Department of Neurology, Georgetown University, Washington, DC 20007
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Peter E. Turkeltaub
5Department of Neurology, Georgetown University, Washington, DC 20007
6MedStar National Rehabilitation Hospital, Washington, DC 20007
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Abstract

Aphasia is a prevalent cognitive syndrome caused by stroke. The rarity of premorbid imaging and heterogeneity of lesion obscures the links between the local effects of the lesion, global anatomic network organization, and aphasia symptoms. We applied a simulated attack approach in humans to examine the effects of 39 stroke lesions (16 females) on anatomic network topology by simulating their effects in a control sample of 36 healthy (15 females) brain networks. We focused on measures of global network organization thought to support overall brain function and resilience in the whole brain and within the left hemisphere. After removing lesion volume from the network topology measures and behavioral scores [the Western Aphasia Battery Aphasia Quotient (WAB-AQ), four behavioral factor scores obtained from a neuropsychological battery, and a factor sum], we compared the behavioral variance accounted for by simulated poststroke connectomes to that observed in the randomly permuted data. Global measures of anatomic network topology in the whole brain and left hemisphere accounted for 10% variance or more of the WAB-AQ and the lexical factor score beyond lesion volume and null permutations. Streamline networks provided more reliable point estimates than FA networks. Edge weights and network efficiency were weighted most highly in predicting the WAB-AQ for FA networks. Overall, our results suggest that global network measures provide modest statistical value beyond lesion volume when predicting overall aphasia severity, but less value in predicting specific behaviors. Variability in estimates could be induced by premorbid ability, deafferentation and diaschisis, and neuroplasticity following stroke.

SIGNIFICANCE STATEMENT Poststroke, the remaining neuroanatomy maintains cognition and supports recovery. However, studies often use small, cross-sectional samples that cannot fully model the interactions between lesions and other variables that affect networks in stroke. Alternate methods are required to account for these effects. “Simulated attack” models are computational approaches that apply virtual damage to the brain and measure their putative consequences. Using a simulated attack model, we estimated how simulated damage to anatomic networks could account for language performance. Overall, our results reveal that global network measures can provide modest statistical value predicting overall aphasia severity, but less value in predicting specific behaviors. These findings suggest that more theoretically precise network models could be necessary to robustly predict individual outcomes in aphasia.

  • aphasia
  • network
  • neuroimaging
  • simulated attack
  • stroke
  • WAB

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The Journal of Neuroscience: 42 (24)
Journal of Neuroscience
Vol. 42, Issue 24
15 Jun 2022
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Simulated Attack Reveals How Lesions Affect Network Properties in Poststroke Aphasia
John D. Medaglia, Brian A. Erickson, Dorian Pustina, Apoorva S. Kelkar, Andrew T. DeMarco, J. Vivian Dickens, Peter E. Turkeltaub
Journal of Neuroscience 15 June 2022, 42 (24) 4913-4926; DOI: 10.1523/JNEUROSCI.1163-21.2022

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Simulated Attack Reveals How Lesions Affect Network Properties in Poststroke Aphasia
John D. Medaglia, Brian A. Erickson, Dorian Pustina, Apoorva S. Kelkar, Andrew T. DeMarco, J. Vivian Dickens, Peter E. Turkeltaub
Journal of Neuroscience 15 June 2022, 42 (24) 4913-4926; DOI: 10.1523/JNEUROSCI.1163-21.2022
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Keywords

  • aphasia
  • network
  • neuroimaging
  • simulated attack
  • stroke
  • WAB

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