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.
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.
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).
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.
INCLUDE WHEN CITING Published online September 9, 2016; DOI: 10.3171/2016.5.JNS16243.
Alm PA, Cluttering: a neurological perspective. Ward D, Scott KS: Cluttering—A Handbook of Research, Intervention, and Education Hove, UK, Psychology Press, 2011. 3–28
Brown A, Docherty GJ: Phonetic variation in dysarthric speech as a function of sampling task. Eur J Disord Commun 30:17–35, 1995
Butson CR, Cooper SE, Henderson JM, McIntyre CC: Patient-specific analysis of the volume of tissue activated during deep brain stimulation. Neuroimage 34:661–670, 2007
Carpenter MB: Core Text of Neuroanatomy Baltimore, Williams and Wilkins, 1991. 1–478
Coenen VA, Allert N, Paus S, Kronenbürger M, Urbach H, Mädler B: Modulation of the cerebellothalamo-cortical network in thalamic deep brain stimulation for tremor: a diffusion tensor imaging study. Neurosurgery 75:657–670, 2014
Coenen VA, Mädler B, Schiffbauer H, Urbach H, Allert N: Individual fiber anatomy of the subthalamic region revealed with diffusion tensor imaging: a concept to identify the deep brain stimulation target for tremor suppression. Neurosurgery 68:1069–1076, 2011
Fahn S, Elton RL, UPDRS Program Members, Unified Parkinson's Disease Rating Scale. Fahn S, Marsden CD, Goldstein M, et al.: Recent Developments in Parkinson's Disease Florham Park, NJ, Macmillan Healthcare Information, 1987. 2:153–163
Hassler R, Mundinger F, Riechert T: Stereotaxis in Parkinson Syndrome. Berlin, Springer, 1979. 2–45
Hu X, Zhang J, Jiang X, Zhou C, Wei L, Yin X, et al.: Decreased interhemispheric functional connectivity in subtypes of Parkinson's disease. J Neurol 262:760–767, 2015
Hustad KC, Dardis CM, McCourt KA: Effects of visual information on intelligibility of open and closed class words in predictable sentences produced by speakers with dysarthria. Clin Linguist Phon 21:353–367, 2007
Kitagawa M, Murata J, Uesugi H, Kikuchi S, Saito H, Tashiro K, et al.: Two-year follow-up of chronic stimulation of the posterior subthalamic white matter for tremor-dominant Parkinson's disease. Neurosurgery 56:281–289, 2005
Klostermann F, Ehlen F, Vesper J, Nubel K, Gross M, Marzinzik F, et al.: Effects of subthalamic deep brain stimulation on dysarthrophonia in Parkinson's disease. J Neurol Neurosurg Psychiatry 79:522–529, 2008
Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, et al.: Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 349:1925–1934, 2003
Marras C, Rochon P, Lang AE: Predicting motor decline and disability in Parkinson disease: a systematic review. Arch Neurol 59:1724–1728, 2002
Max L, Guenther FH, Gracco VL, Ghosh SS, Wallace ME: Unstable or insufficiently activated internal models and feedback-biased motor control as sources of dysfluency: A theoretical model of stuttering. Cont Iss Comm Sci Dis 31:105–122, 2004
Morel A: Stereotactic Atlas of the Human Thalamus and Basal Ganglia Boca Raton, FL, CRC Press, 2007. 1–160
Narayana S, Jacks A, Robin DA, Poizner H, Zhang W, Franklin C, et al.: A noninvasive imaging approach to understanding speech changes following deep brain stimulation in Parkinson's disease. Am J Speech Lang Pathol 18:146–161, 2009
Pinto S, Thobois S, Costes N, Le Bars D, Benabid AL, Broussolle E, et al.: Subthalamic nucleus stimulation and dysarthria in Parkinson's disease: a PET study. Brain 127:602–615, 2004
Rajput AH, Voll A, Rajput ML, Robinson CA, Rajput A: Course in Parkinson disease subtypes: A 39-year clinicopathologic study. Neurology 73:206–212, 2009
Ramig LO, Fox C, Sapir S: Parkinson's disease: speech and voice disorders and their treatment with the Lee Silverman Voice Treatment. Semin Speech Lang 25:169–180, 2004
Sabatini U, Boulanouar K, Fabre N, Martin F, Carel C, Colonnese C, et al.: Cortical motor reorganization in akinetic patients with Parkinson's disease: a functional MRI study. Brain 123:394–403, 2000
Samra K, Riklan M, Levita E, Zimmerman J, Waltz JM, Bergmann L, et al.: Language and speech correlates of anatomically verified lesions in thalamic surgery for parkinsonism. J Speech Hear Res 12:510–540, 1969
Santens P, De Letter M, Van Borsel J, De Reuck J, Caemaert J: Lateralized effects of subthalamic nucleus stimulation on different aspects of speech in Parkinson's disease. Brain Lang 87:253–258, 2003
Schaltenbrand G, Wahren W: Atlas for Stereotaxy of the Human Brain ed 2 New York, Thieme, 1977. Plate 27
Schiess MC, Zheng H, Soukup VM, Bonnen JG, Nauta HJ: Parkinson's disease subtypes: clinical classification and ventricular cerebrospinal fluid analysis. Parkinsonism Relat Disord 6:69–76, 2000
Simonyan K, Ostuni J, Ludlow CL, Horwitz B: Functional but not structural networks of the human laryngeal motor cortex show left hemispheric lateralization during syllable but not breathing production. J Neurosci 29:14912–14923, 2009
Skodda S, Rinsche H, Schlegel U: Progression of dysprosody in Parkinson's disease over time—a longitudinal study. Mov Disord 24:716–722, 2009
Sowman PF, Flavel SC, McShane CL, Sakuma S, Miles TS, Nordstrom MA: Asymmetric activation of motor cortex controlling human anterior digastric muscles during speech and target-directed jaw movements. J Neurophysiol 102:159–166, 2009
Tessitore A, Esposito F, Vitale C, Santangelo G, Amboni M, Russo A, et al.: Default-mode network connectivity in cognitively unimpaired patients with Parkinson disease. Neurology 79:2226–2232, 2012
Tommasi G, Krack P, Fraix V, Le Bas JF, Chabardes S, Benabid AL, et al.: Pyramidal tract side effects induced by deep brain stimulation of the subthalamic nucleus. J Neurol Neurosurg Psychiatry 79:813–819, 2008
Tripoliti E, Limousin P, Foltynie T, Candelario J, Aviles-Olmos I, Hariz MI, et al.: Predictive factors of speech intelligibility following subthalamic nucleus stimulation in consecutive patients with Parkinson's disease. Mov Disord 29:532–538, 2014
Tripoliti E, Zrinzo L, Martinez-Torres I, Frost E, Pinto S, Foltynie T, et al.: Effects of subthalamic stimulation on speech of consecutive patients with Parkinson disease. Neurology 76:80–86, 2011
Tripoliti E, Zrinzo L, Martinez-Torres I, Tisch S, Frost E, Borrell E, et al.: Effects of contact location and voltage amplitude on speech and movement in bilateral subthalamic nucleus deep brain stimulation. Mov Disord 23:2377–2383, 2008
Van Lancker Sidtis D, Cameron K, Sidtis JJ: Dramatic effects of speech task on motor and linguistic planning in severely dysfluent parkinsonian speech. Clin Linguist Phon 26:695–711, 2012
Van Lancker Sidtis D, Rogers T, Godier V, Tagliati M, Sidtis JJ: Voice and fluency changes as a function of speech task and deep brain stimulation. J Speech Lang Hear Res 53:1167–1177, 2010
Wang E, Verhagen Metman L, Bakay R, Arzbaecher J, Bernard B: The effect of unilateral electrostimulation of the subthalamic nucleus on respiratory/phonatory subsystems of speech production in Parkinson's disease—a preliminary report. Clin Linguist Phon 17:283–289, 2003
Wildgruber D, Ackermann H, Grodd W: Differential contributions of motor cortex, basal ganglia, and cerebellum to speech motor control: effects of syllable repetition rate evaluated by fMRI. Neuroimage 13:101–109, 2001
Yorkston K, Beukelman D: Assessment of Intelligibility of Dysarthric Speech Austin, TX, Pro-ed, CC Publications, 1984
| All Time | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1118 | 392 | 147 |
| Full Text Views | 2585 | 286 | 2 |
| PDF Downloads | 1628 | 209 | 2 |
| EPUB Downloads | 0 | 0 | 0 |