Speech changes induced by deep brain stimulation of the subthalamic nucleus in Parkinson disease: involvement of the dentatorubrothalamic tract.
OBJECTIVE Patients with Parkinson disease (PD) who undergo subthalamic nucleus (STN) deep brain stimulation (DBS) often develop a deterioration in speech performance, but there is no clear consensus on the specific effects seen or the mechanism involved and little description of the impact of DBS on conversational speech. Furthermore, there has been no fiber tract connectivity analysis to identify the structures potentially modulated by DBS to cause such deficits. The main objective of this study was to quantify spontaneous speech performance and identify potential involvement of the dentatorubrothalamic tract (DRTt) in patients who underwent STN DBS, because this tract has been implicated in speech deterioration. METHODS Spontaneous speech samples were obtained with STN DBS in both on and off modes in 35 patients with PD and assessed across multiple domains. Diffusion tensor imaging tractography seeded from the therapeutic DBS contacts was performed to identify the fiber tracts involved and, specifically, the DRTt. The position of active electrode contacts was assessed relative to that of the STN. RESULTS Fifteen patients with akinetic-rigid (AR) PD and 20 with tremor-dominant (TD) PD subtypes were identified. In the AR-PD subgroup of patients, in whom there was DRTt involvement, 71% demonstrated much better overall speech and largely improved or unchanged fluency in the DBS-off condition. In patients with TD PD with DRTt involvement, 50% demonstrated better overall speech in the off condition, and equivocal results regarding improved or worsened fluency were found. When there was minimal DRTt involvement, 75% of patients with AR PD had better overall speech in the DBS-on condition and better or minimal fluency changes. Similarly, 83% of patients with TD PD with minimal DRTt involvement had better or minimal overall speech and fluency changes in the on condition. More medially placed left electrode contacts were associated with more DRTt involvement in 77% of patients (10 of 13). CONCLUSIONS To the authors' knowledge, this is the first study to have investigated a specific fiber tract involved in STN DBS in different subtypes of PD relative to its impact on spontaneous speech. At optimal therapeutic programming of STN DBS, overall spontaneous speech and fluency were affected more negatively in patients with AR PD than in those with TD PD when there was DRTt involvement. After fiber tract analysis and modeling, it was found that medially positioned left electrode contacts more often involved fibers of the DRTt. If possible, avoidance of the DRTt by using active electrode contacts that are positioned less medially, specifically in patients with AR PD, might result in less speech deterioration.
Department of Neurosurgery, Mischer Neuroscience Institute, and.
Albert J
AJ
Fenoy
Department of Speech-Language Pathology, New York Medical College, Valhalla, New York.
Monica A
MA
McHenry
Department of Neurology, Movement Disorders and Neurodegenerative Disease Program, McGovern Medical School, University of Texas-Houston Health Science Center, Houston, Texas; and.
Mya C
MC
Schiess
D000368:Aged; D046690:Deep Brain Stimulation / Q000379:methods*; D056324:Diffusion Tensor Imaging; D005260:Female; D006801:Humans; D008297:Male; D008875:Middle Aged; D009434:Neural Pathways / Q000000981:diagnostic imaging / Q000503:physiopathology; D010300:Parkinson Disease / Q000000981:diagnostic imaging / Q000503:physiopathology / Q000628:therapy*; D013060:Speech / Q000502:physiology*; D020531:Subthalamic Nucleus / Q000000981:diagnostic imaging / Q000503:physiopathology*
AR = akinetic-rigid; DBS = deep brain stimulation; DRT = relatively more DRTt involvement; DRTt = dentatorubrothalamic tract; DTI = diffusion tensor imaging; NS = nonsignificant; PD = Parkinson disease; Parkinson disease; STN = subthalamic nucleus; TD = tremor-dominant; VTA = volume of tissue activated; deep brain stimulation; dentatorubrothalamic tract; functional neurosurgery; minDRT = minimal DRTt involvement; speech effects; tractography