Developmental Stuttering and Parkinson's Disease: the Evects Of

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776 J Neurol Neurosurg Psychiatry 1999;66:776–778 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.66.6.776 on 1 June 1999. Downloaded from

SHORT REPORT

Developmental stuttering and Parkinson’s disease: the eVects of levodopa treatment

JeVrey M Anderson, John D Hughes, Leslie J Gonzalez Rothi, Gregory P Crucian, K M Heilman

Abstract bradykinesia, akinesia, and a resting tremor. The eVects of dopamine on developmental His Parkinson’s disease was somewhat atypical stuttering was studied in a 44 year old man because it started at the age of 31 and at the with developmental stuttering and Par- time of testing he was unable to walk without kinson’s disease during three levodopa support. He also reported a lifelong history of “on” periods and three “oV” periods. developmental stuttering that had begun dur- When compared with the “oV” periods, ing early childhood. The patient reported no during the “on”’ periods he demonstrated family history of movement disorders. At the an increase of speech dysfluencies. These time of testing he was on a regiment of findings lend support to the dopamine carbidopa-levodopa (25/100) three times a day hypothesis of developmental stuttering. (5 00 am, 10 00 am, and 3 00 pm). Behaviour- (J Neurol Neurosurg Psychiatry 1999;66:776–778) ally during carbidopa-levodopa treatment the patient oscillated between “on” periods charac- Keywords: stuttering; Parkinson’s disease; dopamine terised by moderate/severe stuttering and agonists dyskinesias, but with mild or little bradykinesia, tremors, or rigidity, and “oV” periods The cause of developmental stuttering is with mild stuttering, no dyskinesias, but with unknown; however, the neuroleptic drug ha- severe resting tremors (more severe distally loperidol decreases speech dysfluencies.1–3 The than proximally), akinesia, bradykinesia, and eYcacy of haloperidol may be due to its rigidity. Because he was unable to walk and was psychotrophic eVects or an alteration of the confined to a wheelchair when either “on” or underlying pathophysiological mechanisms. “oV” levodopa, his disability was graded as a Department of stage V using the Hoehn and Yahr criteria.8 Neurology, University Haloperidol blocks dopaminergic receptors, of Florida College of D2 more than D1, and developmental stutter- During testing, all “on” sessions occurred http://jnnp.bmj.com/ Medicine ing might be related to a hyperactive dopamin- about 1 hour after a dose of carbidopa- J M Anderson ergic state.24 levodopa and all “oV” sessions occurred no J D Hughes sooner than 4 hours after the last dose of L J Gonzalez Rothi Patients with Parkinson’s disease often show a hypokinetic dysarthria,5 hypophonia, and carbidopa-levodopa. G P Crucian The patient reported an automobile accident K M Heilman monotonous pitch, but typically they do not stutter. However, palilalia, another disorder of 26 years before our testing in which he may Services of Neurology speech fluency, may be associated with Parkin- have had a brief loss of consciousness. Kenneth M Heilman son’s disease.6 Developmental stuttering, un- However, his stuttering predated his accident on September 24, 2021 by guest. Protected copyright. like palilalia, is associated with speech repeti- and his speech dysfluencies did not increase or Services of Research decrease after the accident. Recent MRI dem- J M Anderson tions of the initial phonemes and also co- occurs with speech blocks.7 The patient we onstrated only mild cortical atrophy. Services of Audiology report on had developmental stuttering, but and Speech Pathology, did not show palilalia. Methods Veterans Levodopa treatment relieves many of the ANALYSIS OF SPEECH DYSFLUENCIES Administration symptoms of Parkinson’s disease. Dopaminer- Medical Center, The patient’s speech was tested during six Gainesville, Florida, gic treatment seems to increase motor activa- separate sessions; three “on” periods, and three USA tion and it might be expected that levodopa “oV” periods. The “on” and “oV” sessions var- L J Gonzalez Rothi treatment would increase speech fluency or ied from morning to afternoon. The same have no eVect. We report on a patient with examiner, a speech-language pathologist, Correspondence to: developmental stuttering and Parkinson’s dis- Dr JeVrey M Anderson, tested the patient during these six occasions. Research Service No151, ease that provided us an opportunity to study The examiner asked the subject to tell com- VAMC, 1601 SW Archer the eVects of levodopa on speech fluency dur- mon fairy tales randomly selected from the fol- Road, Gainesville, FL 32608, ing “on” and “oV” periods. USA. Telephone 001 352 lowing list; Cinderella, Little Red Riding 376 1611 ext 6943; fax 001 Hood, Jack and the Beanstalk, or Pinocchio. 352 374 6000; email Case report The sessions were audiotaped and a written [email protected]fl.edu A 44 year old right handed man was referred transcript was created from these tapes. Two Received 2 Septembr 1998 for the pharmacological management of his raters were provided with the written tran- Accepted 14 October 1998 Parkinson’s disease that included rigidity, script, listened to the audiotapes of the “on” Developmental stuttering and Parkinson’s disease 777 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.66.6.776 on 1 June 1999. Downloaded from

and “oV” sessions (in an randomised order) and marked on the transcript each dysfluent 30 On sessions episode. These raters were unaware or blinded 25 to the patient’s clinical state and the research Off sessions question. The raters computed the total 20 number of dysfluencies produced per session 15 as well as the type of speech dysfluencies 10 produced by the subject including speech blocks, initial phoneme repetitions, and the 5 presence of extraneous interjections or filler 0 1 2 3

words. These dysfluencies were totalled for Dysfluencies (n/100 syllables) each rater and the scores for each session were Sessions averaged. A speech-language pathologist com- Dysfluencies produced during on and oV levodopa sessions. piled the number of syllables produced during each session and the rate of dysfluencies this patient’s stuttering seemed to be worse produced for each 100 syllables was calculated. during his “on” periods than it was in his “oV” A speech block was defined as a significant, periods. non-natural pause or interruption. An initial The neuromuscular activities that support phoneme repetition was defined as the re- speech production are complex and the peated production of the initial speech sound. mechanisms inducing stuttering are not en- A filler word was defined as an extraneous tirely known. Nudelman et al in an engineering interjection such as “ah”. based,10 motor control theory of speech production, propose the existence of two main nested feedback loops, an outer “linguistic Results loop” that decides and monitors what sounds The interrater agreement between the two are to be made, and an inner “phonatory loop” judges for the overall average rate of speech that is involved with motor programming of the dysfluencies produced per minute during “on” vocal apparatus. Nudelman 10 argue that and “oV” sessions was greater than 90% et al stuttering can be modelled as a momentary ( =0.91). A non-parametric Friedman test was r instability in the system whenever the timing used to compare the dysfluency rate per 100 between these two loops is momentarily syllables. The dysfluency rate during “on” ses- disrupted. Although this model is not anatomi- sion 1 was significantly diVerent when com- cally based, the outer linguistic loop is likely pared to the “oV” session 1 rate (p<0.05). The supported by cortical areas in the dominant “dysfluency rate per 100 syllables during “on” hemisphere’s perisylvian areas, whereas the session 2 when compared to “oV” session 2 was inner phonatory loop is likely supported by the not significantly diVerent (p=0.31), and the dominant hemisphere’s frontal cortex, supple- dysfluency rate produced during “on” session 3 mentary motor area, and striatum via corticos- was also not significantly diVerent (p=1.00) triatothalamocortical circuits.10 11 from those produced during “oV” session 3. Nudelman 12 have suggested that the The average rate of the production of words et al neural processing in the outer linguistic loop

per minute for the three “on” sessions was 73.2 http://jnnp.bmj.com/ (likely mediated by language cortex) is slowed (SEM 5.3), whereas during the three “oV” ses- in stutterers. In the absence of adequate sions the average rate was 73.1 (SEM 8.8). A dopamine there is putamenal dysfunction. The paired test of the rate of words produced each t putamenal dysfunction associated with Parkin- minute during the three “on” sessions, was not son’s disease may slow down the cortical basal significantly diVerent (p=0.99) from the rate ganglia circuit supporting speech production. during the three “oV” sessions. The most commonly occurring motor speech disorder in Parkinson’s disease is hypokinetic Discussion dysarthria marked by a decrease in the on September 24, 2021 by guest. Protected copyright. These results suggest that our patient’s stutter- amplitude of orolingual muscular movements ing was more severe with carbidopa-levodopa and decreased respiratory support.13 14 As a treatment. Although his average rate of word result “speech hastening” may occur that is production remained the same during both analogous to a festinating petit pas gait of Par- “on” and “oV” sessions, during “on” session 1 kinson’s disease. Speech hastening is associated the patient showed severe stuttering as evi- with movements of the articulators producing denced by significant increases in the number poorly articulated, but accelerated speech. of sound repetitions, speech blocks, and use of Nudelman et al12 posit that in non- filler words when compared with “oV” session Parkinsonian developmental stutterers, the 1. The subject’s performance across the six outer linguistic loop is slower than the inner trials displayed an adaptation eVect (figure), in phonatory loop. Perhaps the palilalia associated that the repeated production of the same with Parkinson’s disease is induced by a passages was associated with a reduction in the slowing of the inner phonatory loop in overall number of speech dysfluencies across reference to the outer linguistic loop. trials. This adaptation eVect is characteristic of By contrast with patients with palilalia, developmental stuttering.7 perhaps during this patient’s “on” sessions, Koller reported six patients with extrapy- while the outer loop remains slowed, the inner ramidal disease and dysfluent speech.9 In one phonatory loop becomes accelerated, due to case Koller noted that the patient had an “on- the putamenal receptors receiving more oV” phenomena.9 Although not formally tested dopamine, resulting in speech dysfluencies. 778 Anderson, Hughes, Gonzalez Rothi, et al J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.66.6.776 on 1 June 1999. Downloaded from

However, during “oV” sessions his baseline 3 Burns D, Brady JP, Kuruvilla K. The acute eVect of haloperidol and apomorphine on the severity of stuttering. speech dysfluencies, although still present, are Biology Psychiatry 1978;13:255–64. diminished because with reduced dopamine 4 Waddington JL, O-Boyld KM. Drugs acting on brain the subcortical inner phonatory loop is slowed dopamine receptors. Pharmacol Ther 1989;43:1–52. 5 Illes J, Metter EJ, Hanson WR, et al. Language production and therefore less out of synchrony with the in Parkinson’s disease: acoustic and linguistic considera- slowed outer linguistic loop. tions. Brain Lang 1988;33:146–60. 6 Boller F, Albert M, Denes F. Palilalia. Br J Disord Commun Dopamine blockers such as haloperidol may 1975;10:92–7. also slow the inner phonatory loop and help 7 Bloodstein O. A handbook on stuttering. San Diego, CA: stutterers to re-establish synchrony. Unfortu- Singular Publishing, 1995. 8 Hoehn MM, Yahr MD. Parkinsonism: onset, progression nately haloperidol was not well tolerated by and mortality. Neurology 1967;17:427–42. stutterers.23 However, more recent dopamine 9 Koller WC. Dysfluency (stuttering) in extrapyramidal disease. Arch Neurol 1983;40:175–7. antagonists such as risperidone or olanzapine, 10 Nudelman HB, Herbrich BD, Hoyt BD, et al. A with fewer side eVects than haloperidol, may neuroscience model of stuttering. Journal of Fluency Disor- provide a tolerable treatment option for devel- ders 1989;14:399–427. 11 Alexander GE, DeLong MR, Strick PL. Parallel organiza- opmental stutterers. tion of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 1986;9:357–81. 12 Nudelman HB, Herbrich BD, Hess KR, et al. A model of This work was supported by the Veterans Administration phonatory response time of stutters and fluent speakers to Research Service. We thank Dr Kenneth Logan for information frequency-modulated tones. J Acoust Soc Am 1992;92: concerning the assessment of dysfluencies. 1882–8. 13 Hammen VL, Yorkston KM. Speech and pause character- 1 Brady JP. The pharmacology of stuttering: a critical review. istics following speech rate reduction in hypokinetic dysar- Am J Psychatry 1991;148:1309–16. thria. J Commun Disord 1996;29:429–44. 2 Rosenberger PB, Wheelden JA, Kalokin M. The eVect of 14 Solomon NP Hixon TJ. Speech breathing in Parkinson’s haloperidol on stuttering. Am J Psychiatry 1976;133:331–4. disease. J Speech Hear Res 1993;36:294–310. http://jnnp.bmj.com/ on September 24, 2021 by guest. Protected copyright.