The relationship between dorsal stream connections to the caudate and verbal fluency in Parkinson disease

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ORIGINAL RESEARCH

The relationship between dorsal stream connections to the caudate and verbal fluency in Parkinson disease Federico Rodriguez-Porcel 1 & Janina Wilmskoetter 1 & Christine Cooper 1 & James Andrew Taylor 2 & Julius Fridriksson 3 & Gregory Hickok 4,5 & Leonardo Bonilha 1 Received: 20 August 2019 / Revised: 23 September 2020 / Accepted: 24 September 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Performance in verbal fluency tasks are widely used as a marker of cognitive impairment in Parkinson disease. However, the anatomical substrate of its impairment remains undetermined. Based on the dual-stream language model, we hypothesized cortical input to the subcortical circuitry would be a crucial determinant of fluency. We performed a retrospective study using individual whole-brain structural connectomes derived from 135 individuals with PD and assessed the relationship between white matter integrity and verbal fluency tasks. Controlling for multiple factors, including dysarthria, we observed higher integrity of dorsal stream-caudate connectivity was associated with better letter fluency. This preliminary study indicates the possible dissociation between dorsal and ventral stream connectivity and letter fluency in PD. In addition, it suggests a non-motor role of the frontostriatal fibers in letter fluency. Keywords Fluency . Parkinson disease . Dual Stream Model . Caudate . Frontostriatal

Introduction Communication impairments are common in Parkinson disease (PD) (Smith and Caplan 2018). These include speech Statement of Significance This report is the first one to evaluate the applicability of the dual stream model to understand language impairment in Parkinson disease. In addition, it suggests a non-motor role of the frontostriatal fibers in letter fluency. Electronic supplementary material The online version of this article (https://doi.org/10.1007/s11682-020-00407-2) contains supplementary material, which is available to authorized users. * Federico Rodriguez-Porcel [email protected] 1

Department of Neurology, Medical University of South Carolina, 208b Rutledge Av., Charleston, SC 29403, USA

2

Center for Biomedical Imaging, Medical University of South Carolina, Charleston, SC, USA

3

Department of Communication Sciences and Disorders, University of South Carolina, Columbia, SC, USA

4

Department of Cognitive Sciences, University of California, Irvine, Irvine, CA, USA

5

Department of Language Science , University of California, Irvine, Irvine, CA, USA

impairments, often characterized by hypophonic dysarthria, and language deficits, including word-finding and complex grammar comprehension (Smith and Caplan 2018). Verbal fluency tasks are widely used in the assessment of patients with PD (Henry and Crawford 2004). Performance in verbal fluency tasks are used in the early detection and monitoring of cognitive impairment in PD, particularly in the context of subthalamic nucleus deep brain stimulation, where declines in verbal fluency are commonly reported adv