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Longitudinal fMRI task reveals neural plasticity in default mode network with disrupted executive-default coupling and selective attention after traumatic brain injury

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Abstract

Executive dysfunctions are common in individuals with Traumatic Brain Injury (TBI). However, change in functional neural coupling of default and executive networks in the post-acute phase (≥ 1 month after injury) patients over time has yet to be understood. During a 5-week observation period, we examined changes in the goal-oriented executive function networks in 20 TBI participants, using a face/scene matching 1-back fMRI task (Chen et al. 2011). We conducted multivariate pattern analysis to assess working memory and visual selective attention, followed by a repeat-measures ANOVA to examine longitudinal changes, with a cluster FDR at p = .001. Results showed that task accuracy significantly improved after follow-up. Significantly increased activity patterns over time were observed in the right dorsolateral prefrontal cortex and right insula. Decreased activity patterns were seen in the left posterior cingulate cortex (PCC), bilateral precuneus, right inferior occipital gyrus and right temporo-occipital junction. Improvement in task accuracy correlated with decreased activity patterns in the PCC (r = −0.478, p = 0.031) and temporo-occipital junction (r = −0.592, p = 0.006), which were interpreted as neural plastic changes. However, we did not observe the default mode network (DMN)-executive network decoupling during task performance that is found in other studies. These results suggest that fMRI of attentional task performance could serve as a potential biomarker for neural plasticity of selective attention in TBI patients in the post-acute phase.

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Acknowledgements

The authors wish to thank the participating patients and a number of individuals who made this study possible, in particular: Anthony J.-W. Chen, MD for sharing the task design; Thorsten Kahnt, PhD for MVPA guidance; Amy Anne Herrold, PhD and James L Reilly, PhD for TBI consultation.

Funding

This work was supported by a grant from the Taiwan Ministry of Science and Technology (NSC 103–2420-H-007-004-MY2) to Fan-pei Gloria Yang.

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  1. Lei Wang and Fan-pei Gloria Yang Equal contribution co-senior author.

Authors and Affiliations

  1. National Defense Medical Center, School of Medicine, Taipei, Taiwan

    Shun-Chin Jim Wu

  2. Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, Chicago, IL, USA

    Lisanne M. Jenkins, Alexandra C. Apple, Julie Petersen & Lei Wang

  3. National Taiwan University Hospital, Taipei, Taiwan

    Furen Xiao

  4. Center for Cognition & Mind Science, National Tsinghua University, No. 101, Section 2, Kuang-Fu Road, Hsinchu, Taiwan, 30013

    Fan-pei Gloria Yang

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  1. Shun-Chin Jim Wu
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Correspondence to Fan-pei Gloria Yang.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

Disclosures

The task paradigm employed in this study has proved test–retest effects for TBI patients (Chen et al. 2011). In addition, in previous longitudinal studies with N-back tests, task-based fMRI showed robust test-retest effects (Koolschijn et al. 2011; Zanto et al. 2014) and no significant change (Fonville et al. 2015; Mattfeld et al. 2016; Sanchez-Carrion et al. 2008) in healthy adults.

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Wu, SC.J., Jenkins, L.M., Apple, A.C. et al. Longitudinal fMRI task reveals neural plasticity in default mode network with disrupted executive-default coupling and selective attention after traumatic brain injury. Brain Imaging and Behavior 14, 1638–1650 (2020). https://doi.org/10.1007/s11682-019-00094-8

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