Neuropsychology Joanna L. Hutchison University of Texas at Dallas and University of Texas...

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  • Neuropsychology

    Asynchrony in Executive Networks Predicts Cognitive Slowing in Multiple Sclerosis Nicholas A. Hubbard, Joanna L. Hutchison, Monroe P. Turner, Saranya Sundaram, Larry Oasay, Diana Robinson, Jeremy Strain, Travis Weaver, Scott L. Davis, Gina M. Remington, Hao Huang, Bharat B. Biswal, John Hart, Jr., Teresa C. Frohman, Elliot M. Frohman, and Bart Rypma Online First Publication, July 6, 2015. http://dx.doi.org/10.1037/neu0000202

    CITATION Hubbard, N. A., Hutchison, J. L., Turner, M. P., Sundaram, S., Oasay, L., Robinson, D., Strain, J., Weaver, T., Davis, S. L., Remington, G. M., Huang, H., Biswal, B. B., Hart, J., Jr., Frohman, T. C., Frohman, E. M., & Rypma, B. (2015, July 6). Asynchrony in Executive Networks Predicts Cognitive Slowing in Multiple Sclerosis. Neuropsychology. Advance online publication. http://dx.doi.org/10.1037/neu0000202

  • Asynchrony in Executive Networks Predicts Cognitive Slowing in Multiple Sclerosis

    Nicholas A. Hubbard University of Texas at Dallas

    Joanna L. Hutchison University of Texas at Dallas and University of Texas

    Southwestern Medical Center

    Monroe P. Turner, Saranya Sundaram, Larry Oasay, Diana Robinson, Jeremy Strain, and Travis Weaver

    University of Texas at Dallas

    Scott L. Davis Southern Methodist University

    Gina M. Remington and Hao Huang University of Texas Southwestern Medical Center

    Bharat B. Biswal New Jersey Institute of Technology

    John Hart Jr. University of Texas at Dallas and University of Texas

    Southwestern Medical Center

    Teresa C. Frohman and Elliot M. Frohman University of Texas Southwestern Medical Center

    Bart Rypma University of Texas at Dallas and University of Texas Southwestern Medical Center

    Objective: Cognitive slowing is a core neuropsychological symptom of Multiple Sclerosis (MS). We aimed to assess the extent to which cognitive slowing in MS was predicted by changes in dorsolateral prefrontal networks. Method: We assessed patients with relapsing-remitting MS and healthy controls (HCs) on measures of processing speed. Participants underwent a functional MRI while performing a processing speed task to allow assessment of task-based connectivity. Results: Patients were slower than HCs on the processing speed tasks. Patients showed attenuated connectivity between right and left dorsolateral prefrontal cortex (DLPFC) and task-relevant brain regions compared to HCs during pro- cessing speed task performance. Patients’ connectivity with DLPFC in these group-disparate networks accounted for significant variability in their performance on processing speed measures administered both in and out of the imaging environment. Specifically, patients who had stronger functional connec- tions with DLPFC in group-disparate networks performed faster than patients with weaker connections with DLPFC in group-disparate networks. Conclusion: Results suggest that MS-related cognitive slowing can be accounted for by systemic alterations in executive functional networks.

    Keywords: executive networks, prefrontal cortex, processing speed, fMRI, multiple sclerosis

    Supplemental materials: http://dx.doi.org/10.1037/neu0000202.supp

    Nicholas A. Hubbard, School of Behavioral and Brain Sciences, The Center for BrainHealth, University of Texas at Dallas; Joanna L. Hutchi- son, School of Behavioral and Brain Sciences, The Center for BrainHealth, University of Texas at Dallas and Department of Psychiatry, University of Texas Southwestern Medical Center; Monroe P. Turner, Saranya Sundaram, Larry Oasay, Diana Robinson, Jeremy Strain, and Travis Weaver, School of Behavioral and Brain Sciences, The Center for Brain- Health, University of Texas at Dallas; Scott L. Davis, Department of Applied Physiology and Wellness, Southern Methodist University; Gina M. Remington, Department of Neurology and Neurotherapeutics and De- partment of Ophthalmology, University of Texas Southwestern Medical Center; Hao Huang, Advanced Imaging Research Center and Department of Radiology, University of Texas Southwestern Medical Center; Bharat B. Biswal, Department of Biomedical Engineering, New Jersey Institute of Technology; John Hart Jr., School of Behavioral and Brain Sciences, The

    Center for BrainHealth, University of Texas at Dallas and Department of Psychiatry and Department of Neurology and Neurotherapeutics, Uni- versity of Texas Southwestern Medical Center; Teresa C. Frohman, Department of Neurology and Neurotherapeutics, University of Texas Southwestern Medical Center; Elliot M. Frohman, Department of Neu- rology and Neurotherapeutics and Department of Ophthalmology, Uni- versity of Texas Southwestern Medical Center; Bart Rypma, School of Behavioral and Brain Sciences, The Center for BrainHealth, University of Texas at Dallas and Department of Psychiatry, University of Texas Southwestern Medical Center.

    Dr. Hao Huang is now at the Department of Radiology, University of Pennsylvania, Philadelphia, Pennsylvania.

    Correspondence concerning this article should be addressed to Nicholas A. Hubbard, School of Behavioral and Brain Sciences, The Center for BrainHealth, University of Texas at Dallas, 2200 West Mockingbird Lane, Dallas, TX 75235. E-mail: nicholas.hubbard@utdallas.edu

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    Neuropsychology © 2015 American Psychological Association 2015, Vol. 29, No. 4, 000 0894-4105/15/$12.00 http://dx.doi.org/10.1037/neu0000202

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  • Neuropsychological dysfunction accompanies approximately 65% of cases of Multiple Sclerosis (MS; see Genova, Hillary, Wylie, Rypma, & DeLuca, 2009). It is frequently observed that processing speed, the speed with which individuals can execute elementary cognitive operations (Rypma et al., 2006; Salthouse, 1992), is compromised in MS patients (see Rao et al., 2014). Deficits in this basic neuropsychological ability exert deleterious effects upon day-to-day functioning and are reflected in more widespread, higher-order cognitive deficits (e.g., working memory and reasoning; see Ackerman, Beier, & Boyle, 2002; Rypma et al., 2006; Rypma & Prabhakaran, 2009; Salthouse, 1996; Salthouse & Babcock, 1991; Vernon, 1983). To date, however, only two studies have examined the neurofunctional basis of processing speed in MS patients (Genova, Sumowski, Chiaravalloti, Voelbel, & De- Luca, 2009; Leavitt, Wylie, Genova, Chiaravalloti, & DeLuca, 2012), and it is not known whether MS-related processing speed deficits are associated with alterations in functional neural net- works. In the current study, we used functional neuroimaging to assess (a) whether MS-related changes existed in dorsolateral prefrontal networks during processing speed task performance and (b) whether MS-related changes in these networks predicted cog- nitive slowing.

    In fMRI research, functional connectivity techniques permit observation of interregional fluctuations of blood-oxygen-level dependent (BOLD) activity. Anatomical regions, or nodes, are said to form a functionally connected network when BOLD activity across nodes shows a high degree of temporal coherence (i.e., synchrony; Joel, Caffo, van Zijl, & Pekar, 2011). Functional con- nectivity analyses have shown reduced synchronous activity in MS patients compared to healthy controls (HCs) during both resting brain states (e.g., Bonavita et al., 2011; Cruz-Gómez, Ventura- Campos, Belenguer, Ávila, & Forn, 2014; Janssen, Boster, Patter- son, Abduljalil, & Prakash, 2013; Roosendaal et al., 2010; Saini et al., 2004) and during task engagement (e.g., Au Duong et al., 2005; Cader, Cifelli, Abu-Omar, Palace, & Matthews, 2006; Passamonti et al., 2009). For instance, Cruz-Gómez and colleagues (2014) demonstrated that cognitively impaired MS patients showed less functional connectivity in resting networks than their unimpaired cohorts. Similarly, Cader and colleagues (2006) showed that, dur- ing working memory task performance, dorsolateral prefrontal cortex (DLPFC) was less functionally connected with other task- relevant regions in MS patients relative to HCs

    DLPFC has been characterized as an information-processing control center that mediates executive cognitive processes (e.g., Curtis & D’Esposito, 2003; Hillary, Genova, Chiaravalloti, Rypma, & DeLuca, 2006; Hubbard, Hutchson et al., 2014; Rypma et al., 2006; Rypma & Prabhakaran, 2009). This executive center interacts with memory, motor, and sensory structures to direct thought and action in accordance with internal goal-states. As such, DLPFC acts as a hub within a rich network of connections; it receives input from sensory projections and has direct connec- tions with regions relevant to behavioral response (e.g., premotor regions, frontal eye fields, cerebellum, and basal ganglia; see Miller & Cohen, 2001). Thus, both the magnitude of activity in DLPFC and connectivity with DLPFC have been implicated in processing speed and higher order cognitive processes (Hillary et al., 2006; Rypma et al., 2006; Rypma & Prabhakaran, 2009).

    One study has examined processing speed performance and the magnitude of BOLD activity in MS pa