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Phenomenology of abnormal movements in stuttering
Parkinsonism and Related Disorders 14 (2008) 415e419 www.elsevier.com/locate/parkreldis
Phenomenology of abnormal movements in stuttering Patricio Riva-Posse, Laura Busto-Marolt, Angeles Schteinschnaider, Lucia Martinez-Echenique, Angel Cammarota, Marcelo Merello* Neuroscience Department, Movement Disorders Section, Rau´l Carrea Institute for Neurological Research, FLENI, Monta~neses 2325, 1428AQK, Ciudad de Buenos Aires, Argentina Received 25 July 2007; received in revised form 5 November 2007; accepted 11 November 2007
Abstract Background: Stuttering is often accompanied by involuntary movements, abnormal gestures or changes in facial expression. Objective: To describe the incidence and phenomenology of abnormal movements (AMs) in stuttering patients. Materials and methods: Eighty-five consecutive patients with stuttering and 119 normal controls videotaped and subsequently reviewed, in which AMs were classified as voluntary or involuntary, and as concurrent or unrelated to speech. Movement phenomenology was correlated with disease severity. Results: Of 85 stuttering patients studied, 51.7% had AMs and 22 more than one AM. Sixty-six different AMs were identified, of which 83.3% occurred during speech, 72.7% were classified as involuntary, and 27.2% as voluntary. Of 38 involuntary movements concurrent to speech, 25 were originally perceived as voluntary, but had since become involuntary through repeated use during stuttering. All involuntary movements not concurrent to speech fulfilled criteria for tics. Conclusion: AMs occurring during stuttering were not always involuntary; movements not concurrent with speech clearly fulfilled clinical criteria for tics and were similar in incidence to normal controls. Inverse correlation was found between conscious control of movement during speech and stuttering severity. Many involuntary movements occurring during speech were clearly referred by patients as initially voluntary early on in the development of their speech disorder (starters or unblockers), underlining the importance of repetitive use of complex motor sequences as a source for putative involuntary movement genesis. Ó 2008 Elsevier Ltd. All rights reserved. Keywords: Stuttering; Stammering; Tics; Involuntary movements; Basal ganglia
1. Introduction Stuttering or stammering is defined as the spasmodic repetition or prolongation of sounds and syllables together with involuntary pauses or blocks, which markedly impair the fluency of speech. Developmental stuttering, a sporadic disorder usually beginning in early childhood around ages 2e4, has been described in all cultures although its causes remain unknown [1]. The accepted incidence for persistent developmental stuttering is about 1%, although higher in preschool populations [2], and three times more common in boys than in girls.
* Corresponding author. Tel.: þ54 11 5777 3200; fax: þ54 11 5777 3209. E-mail address: [email protected] (M. Merello). 1353-8020/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.parkreldis.2007.11.006
Hereditary factors also appear to influence stuttering [3], a family history of the disorder is often observed, and if one monozygotic twin stutters there is a 90% chance the other twin will also, a possibility reduced to 20% in dizygotic twins [4]. Not only does stuttering per se seem to have a genetic link, but the likelihood of spontaneous recovery or chronic development of the disorder also appears to be hereditary. People who stutter usually accompany their speech with involuntary movements, abnormal gestures, or changes in facial expression. Mulligan et al. [5] have suggested that the presence of simple and complex motor tics in these patients is related to a common underlying pathophysiology, namely abnormal function of basal ganglia, or their immediate connections. Abnormal movements accompanying stuttering can frequently be more disturbing than the actual dysfluency [6].
e
e n¼0
n¼2
n¼0
Laterocollis jerk (n ¼ 1) Tonic contraction of neck (n ¼ 1)
Facial grimace (n ¼ 2) n¼2
Normal controls
In addition to involuntary movements, stutterers sometimes help phrase initiation by using voluntary movements called ‘‘starter movements’’ such as slapping a leg or making a facial grimace, or ‘‘unblocking movements’’ such as suddenly jerking an arm or the neck to unblock phrases interrupted by stuttering when prolongation or block interferes with normal speech fluency. The present protocol was designed to establish prospectively the incidence, phenomenology and clinical correlates of abnormal movements accompanying stuttering.
Tonic eye closure (n ¼ 4)
P. Riva-Posse et al. / Parkinsonism and Related Disorders 14 (2008) 415e419
n¼4
416
Jerks (n ¼ 1)
e n¼0 n¼1 Trunk
n¼0
n¼0
e ‘‘Rocking jerks’’ (n ¼ 1)
n¼0 Shoulders
n¼2 Laterocollis jerk (n ¼ 2) Retrocollis jerk (n ¼ 4) Clonic ‘‘to-and-fro’’ movements (n ¼ 1) Choreic ‘‘snake-like’’ movements (n ¼ 1)
Dystonic facial grimace (n ¼ 1)
e e
n¼8 Neck
n¼1
Neck jerks (n ¼ 3) Dystonic head tilt (n ¼ 1)
Clonic movements of mouth (n ¼ 4); n¼5 Orofacial
Clonic lateral neck movements (n ¼ 1) Retrocollis jerk (n ¼ 1)
n¼4
n¼2
n¼6
n¼5
Always involuntary
Tonic eye closure (n ¼ 9) Jerky eye closure (n ¼ 1) Tonic conjugate eye deviation (n ¼ 1) n ¼ 11
2.3.2. Abnormal movement evaluation Videotapes of patients and normal controls were randomly evaluated by the study neurologists for the presence of abnormal movement, while blinded to the speech therapist evaluation of stuttering severity. These were classified and rated according to an in house developed scale as: ocular, orofacial, of the jaw, of the neck, shoulder, trunk, hand or limb, depending on their site of origin; and as tonic, clonic, jerks, dystonic-like or choreiform depending on the type of movement generated (Table 1). Severity was defined according to the degree to which the movement caused listener detraction from the spoken message, and subjectively graded as mild, moderate, or severe.
Initially voluntary
2.3.1. Stuttering evaluation Each videotape was analyzed by both speech therapists. Stuttering severity was assessed using the Stuttering Severity Instrument for Children and Adults (SSI-3) Scale by Glyndon B. Riley [7], and the percentage of stuttered syllables during a given time period and the type of verbal symptoms conforming the stuttering pattern registered.
Concurrent with speech
Patients were videotaped during a structured speech therapy session. All video recordings were at least 5 min long. With the aim of exposing the patients to different settings, videotapes included: 1 e spontaneous speech, 2 e specific task performance with a structured script such as using the phone to make an appointment, inquiring about services at a bank or a school (depending on the age of the patient) and 3 e reading a given text out loud. Stuttering and presence of abnormal movements were evaluated during all the three tasks.
Table 1 Topography and phenomenology of involuntary movements
2.3. Methods
Ocular
One hundred and nineteen controls with comparable demographics, including social and cultural characteristics, consulted from the University of Buenos Aires School of Medicine, a primary school and a rugby club from the same area, consented to participate in the study.
Tonic facial grimace (n ¼ 1) Clonic eyebrow elevations (n ¼ 1) Tonic eyebrow elevation (n ¼ 1) Cloniform jaw openings (n ¼ 1) Dystonic tongue protrusion (n ¼ 1)
2.2. Control group
Blinking (n ¼ 3) Tonic eye closure (n ¼ 2) Conjugate eye deviation (n ¼ 1)
A consecutive series of 85 stuttering patients drawn from individuals spontaneously consulting or referred for diagnosis or treatment to a speech therapy clinic in Buenos Aires were analyzed. All were native Spanish speakers, with no prior history of pharmacological treatment or other neurological conditions other than the stuttering. Patients under the age of 6 were excluded, since preschoolers usually outgrow stuttering of developmental origin. Routine evaluation included a basic neurological examination and a Folstein Mini-mental test. Patients gave consent to being videotaped prior to treatment, and for this material to be used for investigational purposes.
n¼3
Not related to speech
2.1. Patients
Tonic eye closure (n ¼ 1) Repeated blinking (n ¼ 2)
A team comprised of two speech therapists (L.B-M. and L.M-E.) and four movement disorder specialists (M.M., A.C., A.S. and P.R-P) designed and obtained approval from the local ethics committee for the protocol used in this study.
‘‘Facial Hemispasm-like’’ (n ¼ 1) Lip biting (n ¼ 1)
2. Materials and methods
P. Riva-Posse et al. / Parkinsonism and Related Disorders 14 (2008) 415e419 Movements were also classified as speech related (i.e. occurring only during speech) or unrelated to speech. The former were categorized depending on their role, as either help words or phrase initiators (starters), or unblockers when used to unblock interrupted word or phrase emission. During a ‘‘posthoc’’ unstructured interview after revisiting the tapes, patients with movement disorders were asked if they were aware of movement performance executed to improve fluency. If the patient was not, or had no control over these movements these was classified as involuntary. If the patient recognized the need for their use in order to improve fluency then they were classified as voluntary (starter or unblocker). During these interviews an unexpected third group was identified, made up of patients in whom the movement occurred involuntarily but who recognized that early in the course of the disease the movement improving fluency had started out as voluntary. Involuntary movements concurrent to speech were therefore divided into those that had initially been voluntarily and used as starters or unblockers and later incorporated to speech and now expressed involuntarily; and those, which had never been under conscious control (Fig. 1). During this interview clinical criteria for Tourette syndrome were also applied to rule out this diagnosis [8].
3. Statistical analysis Data expressed as mean values standard deviation, were processed using 2-way ANOVA and post hoc paired t-test comparisons. Frequency distributions were calculated using chi square, cells <5 were Yates corrected. Spearman’s rank was used for correlations. All p values were two-tailed and threshold for significance was set at p < 0.05. 4. Results 4.1. Demographic characteristics Mean SD patient population age was 19.95 10.39 years, 67 patients were male (78.82%). Mean SD control group age was 19.59 5.84, and 89 (74.7%) were male. No Patients with Stuttering n=85
Patients with Abnormal Movements n=44
Involuntary Movements n=48 *
Concurrent to speech n=38 *
Not related to speech n=10 * (Fulfilled criteria for tics)
Patients without Abnormal Movements n=41
significant differences in age ( p < 0.74) or gender prevalence were observed between groups (c2 ¼ 0.45, df ¼ 1, p < 0.5). 4.2. Abnormal movements during stuttering Of the 85 patients, 44 (51.7%) had abnormal movements (Fig. 1). A total of 66 abnormal movements were identified. Twenty-two patients presented one abnormal movement, 15 patients two, 5 patients three, 2 patients four, and 1 patient presented five different abnormal movements. No significant differences were found between patients with or without movement disorders regarding age ( p ¼ 0.78) or gender prevalence ( p ¼ 0.9). Of the totality of abnormal movements, 55 (83.3%) occurred during speech, 48 (72.7%) were classified as involuntary, and 38 (79.1%) involuntary movements were concurrent to speech. Of the 18 voluntary movements, two (11.1%) were classified as starters and the rest as unblocking (Table 2). Of the 38 involuntary movements concurrent to speech, 25 were referred by patients as initially voluntary but now involuntarily due to longstanding use during stuttering. All involuntary movements not concurrent with speech observed in this study fulfilled criteria for tics [8], they were abrupt, jerky, repetitive, and involved discrete muscle groups including winking, eye rolling, eyebrow raising, nostril flaring and mouth grimacing, with a total incidence of 7% in stutterers. Topographically, ocular movements were the most frequent, accounting for 30.3% of the total, followed by neck (28.7%), orofacial (22.7%) and hand (10.6%). Ocular movements were all involuntary; 70% tonic and 25% clonic. Orofacial movements were mostly involuntary (60%), and 44% of these were clonic. Neck movements were involuntary in 73.6% of cases and 57.1% were jerks (Table 1). All hand and limb movements were voluntary, whether starter or unblocking. Hand movements accounted for 38.8% of voluntary movements. No correlation was found between age and percentage of stuttered syllables. There was, however, significant correlation between severity of stuttering and percentage of stuttered syllables ( p ¼ 0.017). A direct relationship between severity and number of associated movements ( p ¼ 0.012) was also observed, with involuntary ( p ¼ 0.002) but not voluntary
Voluntary Movements n=18 *
Starters n=2 *
Unblockers n=16 *
Table 2 Topography of voluntary movements (see reference below for description of movements)
Topography Always Involuntary n=13 *
417
Initially Voluntary n=25 *
Fig. 1. Movement disorders associated to stuttering. Some patients presented more than one abnormal movement (indicated by *). This explains why the total n of voluntary plus involuntary movements (n ¼ 66) exceed the number of patients with abnormal movements (n ¼ 44).
Startersa
Unblockersb
Orofacial ¼ 1 Hands ¼ 1
Orofacial ¼ 5 Neck ¼ 5 Hands ¼ 6
a Orofacial: mouth opening with lips inward (n ¼ 1); hands: hand slapping (n ¼ 1). b Orofacial: lip smacking (n ¼ 3), nose frown (n ¼ 1), tongue protrusion (n ¼ 1); neck: anterocollis jerk (n ¼ 3), retrocollis jerk (n ¼ 1), laterocollis posture (n ¼ 1); hands: hand slapping (n ¼ 5), sustained extension of hand (n ¼ 1).
418
P. Riva-Posse et al. / Parkinsonism and Related Disorders 14 (2008) 415e419
( p ¼ 0.56) movements responsible for the majority of the correlation. As expected, involuntary movements concurrent to speech showed significant correlation with stuttering severity ( p ¼ 0.00006). 4.3. Comparison to normal controls None of 119 normal controls presented abnormal movements concurrent with speech. Eight of 119 (6.7%) presented involuntary movements compatible with tics, a prevalence difference not statistically significant from that observed for stutterers (c2 ¼ 1.3, df ¼ 1, p < 0.2). Movements observed included: tonic eye closure (n ¼ 2); frowning (n ¼ 1); tonic eye closure and frowning (n ¼ 1); sustained blinking (n ¼ 2), tonic retrocollis contraction (n ¼ 1) and laterocollis jerk (n ¼ 1). 5. Discussion This study disclosed five main findings: (1) abnormal movements in stuttering are not exclusively involuntary; (2) movements not concurrent to speech clearly fulfill clinical criteria for tics and are present in 7% of stutterers with an incidence comparable to normal controls; (3) movements concurrent to speech can be split into those voluntarily performed to unblock stuttered phrases or to help start speech, and those involuntarily performed; (4) a clear relationship between voluntary movement control concurrent to speech and stuttering severity was observed, with voluntary movements more common in milder cases and involuntary movements in more severe ones; (5) finally, and perhaps most interestingly, many involuntary movements concurrent with speech were clearly referred by patients as initially voluntary (starters or unblockers). Previous studies on movement disorders associated to stuttering [4] considered all movements as involuntary. Clearly movements not concurrent to speech are tics, but movement elicited during stuttering appears more complex in nature. Movements that do not seem to be part of facial expression or related to speech, have long been described as a secondary feature of stuttering and traditionally been viewed as an attempt to overcome difficulty surrounding sound production [9,10]. On the other hand, an alternative explanation for these movements might be to consider them a dystonic syndrome [6] or simple tics, underlining the putative relationship between stuttering and Tourette’s syndrome, and indicating possible basal ganglia involvement in stuttering [11]. Both tics and stuttering can at least partially be suppressed voluntarily, both are influenced by emotional factors and particularly exacerbated under emotional stress [12e14]. Medication used for tic alleviation, particularly neuroleptic drugs, have been reported to improve stuttering [15]. Similarities in behavioral features observed between Tourette’s syndrome and other extrapyramidal movement disorders have also been described in stuttering patients [16,17]. For example, frequency of Obsessive Compulsive Disorder (OCD) observed in
stuttering is similar to that described in Tourette’s syndrome [18], and considerably higher than general OCD prevalence [19]. Cranial dystonias such as oromandibular dystonia, blepharospasm, dystonic adductor dysphonia, lingual dystonia, dystonic dysphagia, spasmodic torticollis, auctioneer dystonia and dystonic writer’s cramp are examples of focal dystonias [20]. All these spasms originating at specific body sites are explicitly sensitive to emotional stress, and in the case of oromandibular dystonia, auctioneer’s dystonia and dystonic writer’s cramp, characteristically action triggered [21]. Abnormal movements associated with stuttering are similar from a phenomenological point of view to those seen in dystonia [22]. Occurrence during attempts at speech is an example of action trigger, similar to tonic jaw muscle contraction frequently provoked by attempts at speaking or eating in dystonic syndromes [23]. Moreover, speech production is often affected by the dystonic process, and impaired respiratory muscle coordination has been shown to occur both in patients with dystonia and persistent developmental stutterers [24,25]. Aside from the phenomenological description, how should involuntary movements present in concurrence with speech be categorized? Are they also tics, or stereotypic because of their coordinated, patterned, rhythmic, purposelesseseemingly-purposeful repetitive characteristics? Or are they mannerisms because they are unique peculiar gestures? Maybe all three movement types are present. Involuntary movements concurrent to speech are difficult to define because of their proven purposeful origin, their complexity and their clear-cut temporal relationship to a stuttered sentence. More investigations will have to be made before proper classification of such movements can be reached. At present, the phenomenological rather than etiological description is favored. As explained previously, many involuntary movements observed during speech in this study were clearly referred by patients as having originally been voluntarily and used as starters or unblockers. The question of whether repeated use of a voluntary motor sequence can make it involuntary remains unanswered. Greater understanding on the role of basal ganglia in implicit learning and habit formation is emerging, although evidence that the same mechanisms are involved in both habit formation and tics is circumstantial [26]. The largest input to the striatum comes from the neocortex and ends at the spiny neurons. Response by these neurons appears to be dependent upon a selective set of perceptual cues and environmental conditions, suggesting that the coordinated striatal response is acquired through learning and experience [27]. Evidence from animal studies suggests the balance between activity of striosome spiny neurons versus those in the striatum matrix may determine vulnerability to dopamine mediated tics and stereotypies [28]. If habits are coordinated ensembles of thought and action, tics or stereotypies could well represent ‘‘prewired bits’’ of behaviour later put together to construct habits [29]. Tic action sequences often arise, like habits, from heightened and selective sensitivity to environmental cues within the body or from the outside world, including subtle premonitions or urges relieved through tic or
P. Riva-Posse et al. / Parkinsonism and Related Disorders 14 (2008) 415e419
compulsion performance. Neural mechanisms underlying tic production remain unclear, preliminary evidence suggests, however, they may involve the same structures underlying habit formation, and that signal recording within the striatum can piece together sequences of motor and cognitive action representation [27]. The habitual repetitive use of starter and unblocker movements during speech may somehow unite them into a single performance unit. In conclusion abnormal movements occurring during stuttering were not always involuntary; movements not concurrent with speech clearly fulfilled clinical criteria for tics and were similar in incidence to normal controls. Inverse correlation was found between conscious control of movement during speech and stuttering severity. Many involuntary movements occurring during speech were clearly referred by patients as initially voluntary, early on in the development of their speech disorder (starters or unblockers), underlining the importance of repetitive use of complex motor sequences as a source for putative involuntary movement genesis. Stuttering could represent a unique clinical model to study the origin of involuntary movements linked to habitual use of an action sequence.
References [1] Salmelin R, Schnitzler A, Schmitz F, Freund H-J. Single word reading in developmental stutterers and fluent speakers. Brain 2000;123:1184e 202. [2] Gordon N. Stuttering: incidence and causes. Dev Med Child Neurol 2002;44:278e82. [3] Sangorrin J. Disfemia o tartamudez. Rev Neurol 2005;41:S43e6. [4] Rosenfield DB. Stuttering. Curr Probl Pediatr 2000;12:1e27. [5] Mulligan HF, Anderson TJ, Jones RD, Williams MJ, Donaldson IM. Tics and developmental stuttering. Parkinsonism Relat Disord 2003; 9:281e9. [6] Kiziltan G, Akalin MA. Stuttering may be a type of action dystonia. Mov Disord 1996;11:278e82. [7] Riley GD. SSI-3 Stuttering Severity Instrument for children and adults. 3rd ed. Pro-Ed; 1994. [8] The Tourette Syndrome Classification Study Group. Definitions and classification of tic disorders. Arch Neurol 1993;50:1013e6. [9] Conture E, Kelly E. Young stutterers’ nonspeech behavior during stuttering. J Speech Hear Res 1991;34:1041e56. [10] Prins D, Lohr F. Behavioral dimensions of stuttered speech. J Speech Hear Res 1972;15:61e71.
419
[11] Abwender DA, Trinidad KS, Jones KR, Como PG, Hymes E, Kurlan R. Features resembling Tourette’s syndrome in developmental stutterers. Brain Lang 1998;62:455e64. [12] Bloodstein O. A handbook on stuttering. 5th ed. San Diego: Singular; 1995. [13] Comings DE, Wu S, Chiu C, Ring RH, Gade R, Ahn C, et al. Polygenic inheritance of Tourette syndrome, stuttering, attention deficit hyperactivity, conduct, and oppositional defiant disorder: the additive and substractive effect of the three dopaminergic genes DRD2, D beta H, and DAT1. Am J Med Genet 1996;67:264e88. [14] Alarcon F, Lees AJ. Stuttering, tic-like facial movements and behavioural disorders. J Neurol 1996;243:105e6. [15] Brady JP. The pharmacology of stuttering: a review. Am J Psychiatry 1991;148:1309e16. [16] Van Borsel J, Vanryckeghem M. Dysfluency and phonic tics in Tourette syndrome: a case report. J Commun Disord 2000;33:227e39. [17] Pauls DL, Leckman JF, Cohen DJ. Familial relationship between Gilles de la Tourette’s syndrome, attention deficit disorder, learning disabilities, speech disorders, and stuttering. J Am Acad Child Adolesc Psychiatry 1993;32:1044e50. [18] Como PG. Obsessiveecompulsive disorder in Tourette’s syndrome. In: Adv Neurol, vol. 65. New York: Raven Press; 1995. pp. 281e91. [19] Karno M, Golding JM, Sorenson SB, Burnam MA. The epidemiology of obsessiveecompulsive disorder in five US communities. Arch Gen Psychiatry 1988;45:1094e9. [20] Marsden CD. The problem of adult-onset idiopathic torsion dystonia and other isolated dyskinesias in adult life (including blepharospasm, oromandibular dystonia, dystonic writer’s cramp, and torticollis, or axial dystonia). In: Eldridge R, Fahn S, editors. Dystonia. Adv Neurol, vol. 14. New York: Raven Press; 1976. p. 259e76. [21] Geyer HL, Bressman SB. The diagnosis of dystonia. Lancet Neurol 2006;5:780e90. [22] Mahr G, Leith W. Stuttering after a dystonic reaction. Psychosomatics 1990;31:465. [23] Lagueny A, Caix P, Schuermans P, Julien J. Jaw dystonia triggered by biting into hard food. Mov Disord 1991;6:174e6. [24] LaBlance GR, Rutherford DR. Respiratory dynamics and speech intelligibility in patients with generalized dystonia. J Commun Disord 1991;24:141e56. [25] Zocchi L, Estenne M, Johnston S, Del Ferro L, War ME. Respiratory muscle incoordination in stuttering speech. Am Rev Respir Dis 1990;141:1510e5. [26] Leckman JF, Riddle MA. Tourette’s syndrome: when habit-forming systems form habits of their own? Neuron 2000;28:349e54. [27] Graybiel AM. The basal ganglia and chunking of action repertoires. Neurobiol Learn Mem 1998;70:119e36. [28] Canales JJ, Graybiel AM. A measure of striatal function predicts motor stereotypy. Nat Neurosci 2000;3:377e83. [29] Jog MS, Kubota Y, Connolly CI, Hillegaart V, Graybiel AM. Building neural representations of habits. Science 1999;286:1745e9.
Phenomenology of abnormal movements in stuttering Patricio Riva-Posse, Laura Busto-Marolt, Angeles Schteinschnaider, Lucia Martinez-Echenique, Angel Cammarota, Marcelo Merello* Neuroscience Department, Movement Disorders Section, Rau´l Carrea Institute for Neurological Research, FLENI, Monta~neses 2325, 1428AQK, Ciudad de Buenos Aires, Argentina Received 25 July 2007; received in revised form 5 November 2007; accepted 11 November 2007
Abstract Background: Stuttering is often accompanied by involuntary movements, abnormal gestures or changes in facial expression. Objective: To describe the incidence and phenomenology of abnormal movements (AMs) in stuttering patients. Materials and methods: Eighty-five consecutive patients with stuttering and 119 normal controls videotaped and subsequently reviewed, in which AMs were classified as voluntary or involuntary, and as concurrent or unrelated to speech. Movement phenomenology was correlated with disease severity. Results: Of 85 stuttering patients studied, 51.7% had AMs and 22 more than one AM. Sixty-six different AMs were identified, of which 83.3% occurred during speech, 72.7% were classified as involuntary, and 27.2% as voluntary. Of 38 involuntary movements concurrent to speech, 25 were originally perceived as voluntary, but had since become involuntary through repeated use during stuttering. All involuntary movements not concurrent to speech fulfilled criteria for tics. Conclusion: AMs occurring during stuttering were not always involuntary; movements not concurrent with speech clearly fulfilled clinical criteria for tics and were similar in incidence to normal controls. Inverse correlation was found between conscious control of movement during speech and stuttering severity. Many involuntary movements occurring during speech were clearly referred by patients as initially voluntary early on in the development of their speech disorder (starters or unblockers), underlining the importance of repetitive use of complex motor sequences as a source for putative involuntary movement genesis. Ó 2008 Elsevier Ltd. All rights reserved. Keywords: Stuttering; Stammering; Tics; Involuntary movements; Basal ganglia
1. Introduction Stuttering or stammering is defined as the spasmodic repetition or prolongation of sounds and syllables together with involuntary pauses or blocks, which markedly impair the fluency of speech. Developmental stuttering, a sporadic disorder usually beginning in early childhood around ages 2e4, has been described in all cultures although its causes remain unknown [1]. The accepted incidence for persistent developmental stuttering is about 1%, although higher in preschool populations [2], and three times more common in boys than in girls.
* Corresponding author. Tel.: þ54 11 5777 3200; fax: þ54 11 5777 3209. E-mail address: [email protected] (M. Merello). 1353-8020/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.parkreldis.2007.11.006
Hereditary factors also appear to influence stuttering [3], a family history of the disorder is often observed, and if one monozygotic twin stutters there is a 90% chance the other twin will also, a possibility reduced to 20% in dizygotic twins [4]. Not only does stuttering per se seem to have a genetic link, but the likelihood of spontaneous recovery or chronic development of the disorder also appears to be hereditary. People who stutter usually accompany their speech with involuntary movements, abnormal gestures, or changes in facial expression. Mulligan et al. [5] have suggested that the presence of simple and complex motor tics in these patients is related to a common underlying pathophysiology, namely abnormal function of basal ganglia, or their immediate connections. Abnormal movements accompanying stuttering can frequently be more disturbing than the actual dysfluency [6].
e
e n¼0
n¼2
n¼0
Laterocollis jerk (n ¼ 1) Tonic contraction of neck (n ¼ 1)
Facial grimace (n ¼ 2) n¼2
Normal controls
In addition to involuntary movements, stutterers sometimes help phrase initiation by using voluntary movements called ‘‘starter movements’’ such as slapping a leg or making a facial grimace, or ‘‘unblocking movements’’ such as suddenly jerking an arm or the neck to unblock phrases interrupted by stuttering when prolongation or block interferes with normal speech fluency. The present protocol was designed to establish prospectively the incidence, phenomenology and clinical correlates of abnormal movements accompanying stuttering.
Tonic eye closure (n ¼ 4)
P. Riva-Posse et al. / Parkinsonism and Related Disorders 14 (2008) 415e419
n¼4
416
Jerks (n ¼ 1)
e n¼0 n¼1 Trunk
n¼0
n¼0
e ‘‘Rocking jerks’’ (n ¼ 1)
n¼0 Shoulders
n¼2 Laterocollis jerk (n ¼ 2) Retrocollis jerk (n ¼ 4) Clonic ‘‘to-and-fro’’ movements (n ¼ 1) Choreic ‘‘snake-like’’ movements (n ¼ 1)
Dystonic facial grimace (n ¼ 1)
e e
n¼8 Neck
n¼1
Neck jerks (n ¼ 3) Dystonic head tilt (n ¼ 1)
Clonic movements of mouth (n ¼ 4); n¼5 Orofacial
Clonic lateral neck movements (n ¼ 1) Retrocollis jerk (n ¼ 1)
n¼4
n¼2
n¼6
n¼5
Always involuntary
Tonic eye closure (n ¼ 9) Jerky eye closure (n ¼ 1) Tonic conjugate eye deviation (n ¼ 1) n ¼ 11
2.3.2. Abnormal movement evaluation Videotapes of patients and normal controls were randomly evaluated by the study neurologists for the presence of abnormal movement, while blinded to the speech therapist evaluation of stuttering severity. These were classified and rated according to an in house developed scale as: ocular, orofacial, of the jaw, of the neck, shoulder, trunk, hand or limb, depending on their site of origin; and as tonic, clonic, jerks, dystonic-like or choreiform depending on the type of movement generated (Table 1). Severity was defined according to the degree to which the movement caused listener detraction from the spoken message, and subjectively graded as mild, moderate, or severe.
Initially voluntary
2.3.1. Stuttering evaluation Each videotape was analyzed by both speech therapists. Stuttering severity was assessed using the Stuttering Severity Instrument for Children and Adults (SSI-3) Scale by Glyndon B. Riley [7], and the percentage of stuttered syllables during a given time period and the type of verbal symptoms conforming the stuttering pattern registered.
Concurrent with speech
Patients were videotaped during a structured speech therapy session. All video recordings were at least 5 min long. With the aim of exposing the patients to different settings, videotapes included: 1 e spontaneous speech, 2 e specific task performance with a structured script such as using the phone to make an appointment, inquiring about services at a bank or a school (depending on the age of the patient) and 3 e reading a given text out loud. Stuttering and presence of abnormal movements were evaluated during all the three tasks.
Table 1 Topography and phenomenology of involuntary movements
2.3. Methods
Ocular
One hundred and nineteen controls with comparable demographics, including social and cultural characteristics, consulted from the University of Buenos Aires School of Medicine, a primary school and a rugby club from the same area, consented to participate in the study.
Tonic facial grimace (n ¼ 1) Clonic eyebrow elevations (n ¼ 1) Tonic eyebrow elevation (n ¼ 1) Cloniform jaw openings (n ¼ 1) Dystonic tongue protrusion (n ¼ 1)
2.2. Control group
Blinking (n ¼ 3) Tonic eye closure (n ¼ 2) Conjugate eye deviation (n ¼ 1)
A consecutive series of 85 stuttering patients drawn from individuals spontaneously consulting or referred for diagnosis or treatment to a speech therapy clinic in Buenos Aires were analyzed. All were native Spanish speakers, with no prior history of pharmacological treatment or other neurological conditions other than the stuttering. Patients under the age of 6 were excluded, since preschoolers usually outgrow stuttering of developmental origin. Routine evaluation included a basic neurological examination and a Folstein Mini-mental test. Patients gave consent to being videotaped prior to treatment, and for this material to be used for investigational purposes.
n¼3
Not related to speech
2.1. Patients
Tonic eye closure (n ¼ 1) Repeated blinking (n ¼ 2)
A team comprised of two speech therapists (L.B-M. and L.M-E.) and four movement disorder specialists (M.M., A.C., A.S. and P.R-P) designed and obtained approval from the local ethics committee for the protocol used in this study.
‘‘Facial Hemispasm-like’’ (n ¼ 1) Lip biting (n ¼ 1)
2. Materials and methods
P. Riva-Posse et al. / Parkinsonism and Related Disorders 14 (2008) 415e419 Movements were also classified as speech related (i.e. occurring only during speech) or unrelated to speech. The former were categorized depending on their role, as either help words or phrase initiators (starters), or unblockers when used to unblock interrupted word or phrase emission. During a ‘‘posthoc’’ unstructured interview after revisiting the tapes, patients with movement disorders were asked if they were aware of movement performance executed to improve fluency. If the patient was not, or had no control over these movements these was classified as involuntary. If the patient recognized the need for their use in order to improve fluency then they were classified as voluntary (starter or unblocker). During these interviews an unexpected third group was identified, made up of patients in whom the movement occurred involuntarily but who recognized that early in the course of the disease the movement improving fluency had started out as voluntary. Involuntary movements concurrent to speech were therefore divided into those that had initially been voluntarily and used as starters or unblockers and later incorporated to speech and now expressed involuntarily; and those, which had never been under conscious control (Fig. 1). During this interview clinical criteria for Tourette syndrome were also applied to rule out this diagnosis [8].
3. Statistical analysis Data expressed as mean values standard deviation, were processed using 2-way ANOVA and post hoc paired t-test comparisons. Frequency distributions were calculated using chi square, cells <5 were Yates corrected. Spearman’s rank was used for correlations. All p values were two-tailed and threshold for significance was set at p < 0.05. 4. Results 4.1. Demographic characteristics Mean SD patient population age was 19.95 10.39 years, 67 patients were male (78.82%). Mean SD control group age was 19.59 5.84, and 89 (74.7%) were male. No Patients with Stuttering n=85
Patients with Abnormal Movements n=44
Involuntary Movements n=48 *
Concurrent to speech n=38 *
Not related to speech n=10 * (Fulfilled criteria for tics)
Patients without Abnormal Movements n=41
significant differences in age ( p < 0.74) or gender prevalence were observed between groups (c2 ¼ 0.45, df ¼ 1, p < 0.5). 4.2. Abnormal movements during stuttering Of the 85 patients, 44 (51.7%) had abnormal movements (Fig. 1). A total of 66 abnormal movements were identified. Twenty-two patients presented one abnormal movement, 15 patients two, 5 patients three, 2 patients four, and 1 patient presented five different abnormal movements. No significant differences were found between patients with or without movement disorders regarding age ( p ¼ 0.78) or gender prevalence ( p ¼ 0.9). Of the totality of abnormal movements, 55 (83.3%) occurred during speech, 48 (72.7%) were classified as involuntary, and 38 (79.1%) involuntary movements were concurrent to speech. Of the 18 voluntary movements, two (11.1%) were classified as starters and the rest as unblocking (Table 2). Of the 38 involuntary movements concurrent to speech, 25 were referred by patients as initially voluntary but now involuntarily due to longstanding use during stuttering. All involuntary movements not concurrent with speech observed in this study fulfilled criteria for tics [8], they were abrupt, jerky, repetitive, and involved discrete muscle groups including winking, eye rolling, eyebrow raising, nostril flaring and mouth grimacing, with a total incidence of 7% in stutterers. Topographically, ocular movements were the most frequent, accounting for 30.3% of the total, followed by neck (28.7%), orofacial (22.7%) and hand (10.6%). Ocular movements were all involuntary; 70% tonic and 25% clonic. Orofacial movements were mostly involuntary (60%), and 44% of these were clonic. Neck movements were involuntary in 73.6% of cases and 57.1% were jerks (Table 1). All hand and limb movements were voluntary, whether starter or unblocking. Hand movements accounted for 38.8% of voluntary movements. No correlation was found between age and percentage of stuttered syllables. There was, however, significant correlation between severity of stuttering and percentage of stuttered syllables ( p ¼ 0.017). A direct relationship between severity and number of associated movements ( p ¼ 0.012) was also observed, with involuntary ( p ¼ 0.002) but not voluntary
Voluntary Movements n=18 *
Starters n=2 *
Unblockers n=16 *
Table 2 Topography of voluntary movements (see reference below for description of movements)
Topography Always Involuntary n=13 *
417
Initially Voluntary n=25 *
Fig. 1. Movement disorders associated to stuttering. Some patients presented more than one abnormal movement (indicated by *). This explains why the total n of voluntary plus involuntary movements (n ¼ 66) exceed the number of patients with abnormal movements (n ¼ 44).
Startersa
Unblockersb
Orofacial ¼ 1 Hands ¼ 1
Orofacial ¼ 5 Neck ¼ 5 Hands ¼ 6
a Orofacial: mouth opening with lips inward (n ¼ 1); hands: hand slapping (n ¼ 1). b Orofacial: lip smacking (n ¼ 3), nose frown (n ¼ 1), tongue protrusion (n ¼ 1); neck: anterocollis jerk (n ¼ 3), retrocollis jerk (n ¼ 1), laterocollis posture (n ¼ 1); hands: hand slapping (n ¼ 5), sustained extension of hand (n ¼ 1).
418
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( p ¼ 0.56) movements responsible for the majority of the correlation. As expected, involuntary movements concurrent to speech showed significant correlation with stuttering severity ( p ¼ 0.00006). 4.3. Comparison to normal controls None of 119 normal controls presented abnormal movements concurrent with speech. Eight of 119 (6.7%) presented involuntary movements compatible with tics, a prevalence difference not statistically significant from that observed for stutterers (c2 ¼ 1.3, df ¼ 1, p < 0.2). Movements observed included: tonic eye closure (n ¼ 2); frowning (n ¼ 1); tonic eye closure and frowning (n ¼ 1); sustained blinking (n ¼ 2), tonic retrocollis contraction (n ¼ 1) and laterocollis jerk (n ¼ 1). 5. Discussion This study disclosed five main findings: (1) abnormal movements in stuttering are not exclusively involuntary; (2) movements not concurrent to speech clearly fulfill clinical criteria for tics and are present in 7% of stutterers with an incidence comparable to normal controls; (3) movements concurrent to speech can be split into those voluntarily performed to unblock stuttered phrases or to help start speech, and those involuntarily performed; (4) a clear relationship between voluntary movement control concurrent to speech and stuttering severity was observed, with voluntary movements more common in milder cases and involuntary movements in more severe ones; (5) finally, and perhaps most interestingly, many involuntary movements concurrent with speech were clearly referred by patients as initially voluntary (starters or unblockers). Previous studies on movement disorders associated to stuttering [4] considered all movements as involuntary. Clearly movements not concurrent to speech are tics, but movement elicited during stuttering appears more complex in nature. Movements that do not seem to be part of facial expression or related to speech, have long been described as a secondary feature of stuttering and traditionally been viewed as an attempt to overcome difficulty surrounding sound production [9,10]. On the other hand, an alternative explanation for these movements might be to consider them a dystonic syndrome [6] or simple tics, underlining the putative relationship between stuttering and Tourette’s syndrome, and indicating possible basal ganglia involvement in stuttering [11]. Both tics and stuttering can at least partially be suppressed voluntarily, both are influenced by emotional factors and particularly exacerbated under emotional stress [12e14]. Medication used for tic alleviation, particularly neuroleptic drugs, have been reported to improve stuttering [15]. Similarities in behavioral features observed between Tourette’s syndrome and other extrapyramidal movement disorders have also been described in stuttering patients [16,17]. For example, frequency of Obsessive Compulsive Disorder (OCD) observed in
stuttering is similar to that described in Tourette’s syndrome [18], and considerably higher than general OCD prevalence [19]. Cranial dystonias such as oromandibular dystonia, blepharospasm, dystonic adductor dysphonia, lingual dystonia, dystonic dysphagia, spasmodic torticollis, auctioneer dystonia and dystonic writer’s cramp are examples of focal dystonias [20]. All these spasms originating at specific body sites are explicitly sensitive to emotional stress, and in the case of oromandibular dystonia, auctioneer’s dystonia and dystonic writer’s cramp, characteristically action triggered [21]. Abnormal movements associated with stuttering are similar from a phenomenological point of view to those seen in dystonia [22]. Occurrence during attempts at speech is an example of action trigger, similar to tonic jaw muscle contraction frequently provoked by attempts at speaking or eating in dystonic syndromes [23]. Moreover, speech production is often affected by the dystonic process, and impaired respiratory muscle coordination has been shown to occur both in patients with dystonia and persistent developmental stutterers [24,25]. Aside from the phenomenological description, how should involuntary movements present in concurrence with speech be categorized? Are they also tics, or stereotypic because of their coordinated, patterned, rhythmic, purposelesseseemingly-purposeful repetitive characteristics? Or are they mannerisms because they are unique peculiar gestures? Maybe all three movement types are present. Involuntary movements concurrent to speech are difficult to define because of their proven purposeful origin, their complexity and their clear-cut temporal relationship to a stuttered sentence. More investigations will have to be made before proper classification of such movements can be reached. At present, the phenomenological rather than etiological description is favored. As explained previously, many involuntary movements observed during speech in this study were clearly referred by patients as having originally been voluntarily and used as starters or unblockers. The question of whether repeated use of a voluntary motor sequence can make it involuntary remains unanswered. Greater understanding on the role of basal ganglia in implicit learning and habit formation is emerging, although evidence that the same mechanisms are involved in both habit formation and tics is circumstantial [26]. The largest input to the striatum comes from the neocortex and ends at the spiny neurons. Response by these neurons appears to be dependent upon a selective set of perceptual cues and environmental conditions, suggesting that the coordinated striatal response is acquired through learning and experience [27]. Evidence from animal studies suggests the balance between activity of striosome spiny neurons versus those in the striatum matrix may determine vulnerability to dopamine mediated tics and stereotypies [28]. If habits are coordinated ensembles of thought and action, tics or stereotypies could well represent ‘‘prewired bits’’ of behaviour later put together to construct habits [29]. Tic action sequences often arise, like habits, from heightened and selective sensitivity to environmental cues within the body or from the outside world, including subtle premonitions or urges relieved through tic or
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compulsion performance. Neural mechanisms underlying tic production remain unclear, preliminary evidence suggests, however, they may involve the same structures underlying habit formation, and that signal recording within the striatum can piece together sequences of motor and cognitive action representation [27]. The habitual repetitive use of starter and unblocker movements during speech may somehow unite them into a single performance unit. In conclusion abnormal movements occurring during stuttering were not always involuntary; movements not concurrent with speech clearly fulfilled clinical criteria for tics and were similar in incidence to normal controls. Inverse correlation was found between conscious control of movement during speech and stuttering severity. Many involuntary movements occurring during speech were clearly referred by patients as initially voluntary, early on in the development of their speech disorder (starters or unblockers), underlining the importance of repetitive use of complex motor sequences as a source for putative involuntary movement genesis. Stuttering could represent a unique clinical model to study the origin of involuntary movements linked to habitual use of an action sequence.
References [1] Salmelin R, Schnitzler A, Schmitz F, Freund H-J. Single word reading in developmental stutterers and fluent speakers. Brain 2000;123:1184e 202. [2] Gordon N. Stuttering: incidence and causes. Dev Med Child Neurol 2002;44:278e82. [3] Sangorrin J. Disfemia o tartamudez. Rev Neurol 2005;41:S43e6. [4] Rosenfield DB. Stuttering. Curr Probl Pediatr 2000;12:1e27. [5] Mulligan HF, Anderson TJ, Jones RD, Williams MJ, Donaldson IM. Tics and developmental stuttering. Parkinsonism Relat Disord 2003; 9:281e9. [6] Kiziltan G, Akalin MA. Stuttering may be a type of action dystonia. Mov Disord 1996;11:278e82. [7] Riley GD. SSI-3 Stuttering Severity Instrument for children and adults. 3rd ed. Pro-Ed; 1994. [8] The Tourette Syndrome Classification Study Group. Definitions and classification of tic disorders. Arch Neurol 1993;50:1013e6. [9] Conture E, Kelly E. Young stutterers’ nonspeech behavior during stuttering. J Speech Hear Res 1991;34:1041e56. [10] Prins D, Lohr F. Behavioral dimensions of stuttered speech. J Speech Hear Res 1972;15:61e71.
419
[11] Abwender DA, Trinidad KS, Jones KR, Como PG, Hymes E, Kurlan R. Features resembling Tourette’s syndrome in developmental stutterers. Brain Lang 1998;62:455e64. [12] Bloodstein O. A handbook on stuttering. 5th ed. San Diego: Singular; 1995. [13] Comings DE, Wu S, Chiu C, Ring RH, Gade R, Ahn C, et al. Polygenic inheritance of Tourette syndrome, stuttering, attention deficit hyperactivity, conduct, and oppositional defiant disorder: the additive and substractive effect of the three dopaminergic genes DRD2, D beta H, and DAT1. Am J Med Genet 1996;67:264e88. [14] Alarcon F, Lees AJ. Stuttering, tic-like facial movements and behavioural disorders. J Neurol 1996;243:105e6. [15] Brady JP. The pharmacology of stuttering: a review. Am J Psychiatry 1991;148:1309e16. [16] Van Borsel J, Vanryckeghem M. Dysfluency and phonic tics in Tourette syndrome: a case report. J Commun Disord 2000;33:227e39. [17] Pauls DL, Leckman JF, Cohen DJ. Familial relationship between Gilles de la Tourette’s syndrome, attention deficit disorder, learning disabilities, speech disorders, and stuttering. J Am Acad Child Adolesc Psychiatry 1993;32:1044e50. [18] Como PG. Obsessiveecompulsive disorder in Tourette’s syndrome. In: Adv Neurol, vol. 65. New York: Raven Press; 1995. pp. 281e91. [19] Karno M, Golding JM, Sorenson SB, Burnam MA. The epidemiology of obsessiveecompulsive disorder in five US communities. Arch Gen Psychiatry 1988;45:1094e9. [20] Marsden CD. The problem of adult-onset idiopathic torsion dystonia and other isolated dyskinesias in adult life (including blepharospasm, oromandibular dystonia, dystonic writer’s cramp, and torticollis, or axial dystonia). In: Eldridge R, Fahn S, editors. Dystonia. Adv Neurol, vol. 14. New York: Raven Press; 1976. p. 259e76. [21] Geyer HL, Bressman SB. The diagnosis of dystonia. Lancet Neurol 2006;5:780e90. [22] Mahr G, Leith W. Stuttering after a dystonic reaction. Psychosomatics 1990;31:465. [23] Lagueny A, Caix P, Schuermans P, Julien J. Jaw dystonia triggered by biting into hard food. Mov Disord 1991;6:174e6. [24] LaBlance GR, Rutherford DR. Respiratory dynamics and speech intelligibility in patients with generalized dystonia. J Commun Disord 1991;24:141e56. [25] Zocchi L, Estenne M, Johnston S, Del Ferro L, War ME. Respiratory muscle incoordination in stuttering speech. Am Rev Respir Dis 1990;141:1510e5. [26] Leckman JF, Riddle MA. Tourette’s syndrome: when habit-forming systems form habits of their own? Neuron 2000;28:349e54. [27] Graybiel AM. The basal ganglia and chunking of action repertoires. Neurobiol Learn Mem 1998;70:119e36. [28] Canales JJ, Graybiel AM. A measure of striatal function predicts motor stereotypy. Nat Neurosci 2000;3:377e83. [29] Jog MS, Kubota Y, Connolly CI, Hillegaart V, Graybiel AM. Building neural representations of habits. Science 1999;286:1745e9.