Stuttering A Dynamic Motor Control Disorder

Journal of Fluency Disorders
28 (2003) 273–295
Stuttering: a dynamic motor control disorder

Christy L. Ludlow∗ , Torrey Loucks
Laryngeal and Speech Section, Clinical Neurosciences Program, National Institute
of Neurological Disorders and Stroke, 10 Center Drive MSC 1416,
Bldg. 10 Rm. 5D38, Bethesda, MD 20892-1416, USA
Received 22 July 2003; accepted 29 July 2003
Abstract
The purpose of this review is to determine what neural mechanisms may be dysfunc-
tional in stuttering. Three sources of evidence are reviewed. First, studies of dynamic
inter-relationships among brain regions during normal speech and in persons who stut-
ter (PWS) suggest that the timing of neural activity in different regions may be abnormal
in PWS. Second, the brain lesions associated with acquired stuttering are reviewed. These
indicate that in a high percentage of cases, the primary speech and language regions are not
affected but lesions involve other structures, such as the basal ganglia, which may modulate
the primary speech and language regions. Third, to characterize the motor control disorder
in stuttering, similarities and differences from focal dystonias such as spasmodic dysphonia
(SD) and Tourette’s syndrome (TS) are reviewed. This review indicates that the central
control abnormalities in stuttering are not due to disturbance in one particular brain region
but rather a system dysfunction that interferes with rapid and dynamic speech processing
for production.
Educational objectives: The reader will be able to describe: (1) the similarities and
differences between stuttering and other speech motor control disorders, (2) which brain
lesions are most likely to produce acquired stuttering in adults, and (3) what type of brain
abnormality most likely underlies stuttering.
© 2003 Elsevier Inc. All rights reserved.
Keywords: Brain lesions; Dystonia; Task specific; Spasmodic dysphonia
∗Corresponding author. Tel.: +1-301-496-9366; fax: +1-301-480-0803.

E-mail address: Ludlowc@ninds.nih.gov (C.L. Ludlow).
0094-730X/$ – see front matter © 2003 Elsevier Inc. All rights reserved.
doi:10.1016/j.jfludis.2003.07.001
274 C.L. Ludlow, T. Loucks / Journal of Fluency Disorders 28 (2003) 273–295
1. Purpose
Our purpose is to identify whether particular neural mechanisms are implicated

by the current literature for characterizing stuttering as a neurodevelopmental mo-
tor control disorder. Because speech is a dynamic motor function process, it re-
quires a highly synchronized and adaptive network of neural activity in order to
function without disruption. We will review the following topics in attempting
to fashion an improved understanding of the underlying mechanisms involved in
stuttering.
1. Recent evidence on the rapid interplay between multiple systems during

speech processing
2. How lesions in many different locations in the brain can disrupt fluency
3. The similarity and differences between stuttering and other speech motor
control disorders
2. The rapid interplay between multiple systems required for fluent speech
Speech is a rapid motor control task; movements must occur within a few
milliseconds in order for the listener to perceive the correct message. For example,
vocal fold opening and closing for voice onset and offset during voiceless and
voiced consonant distinctions are less than 20 ms, a time period which is less than
a quarter of the time of any other laryngeal movements (Ludlow & Lou, 1996).
To produce plosive consonants, the airflow must be sealed long enough for the
pressure to build up and then a rapid ballistic opening gesture is needed to provide
the necessary burst of air (Borden & Harris, 1984).
To study brain mechanisms involved in the rapid processing of speech, high
temporal resolution is needed. Previous studies of brain mechanisms involved in
stuttering have used PET scanning which has spatial resolution but poor temporal
resolution; brain activity is studied over a minute or more. These studies have
shown that many different brain regions are associated with speech production;
the left frontal operculum, the right and left sensory and motor regions, the right
and left primary and auditory association areas and several subcortical regions
including the cerebellum, anterior cingulate, thalamus and the putamen (Braun
et al., 1997; Fox et al., 2000). PET scanning, however, cannot provide information
concerning the rapid inter-relationships between neural events in different brain
regions prior to and during speech gestures or stuttered interruptions. Magnetoen-
cephalography (MEG), on the other hand, has the necessary temporal resolution.
This technique can also have some spatial resolution when the recording points
are mapped onto brain images obtained using magnetic resonance imaging (MRI).
Because of high temporal resolution, within milliseconds, this technique can ex-
amine the dynamic relationships between different brain regions during normal
speech and language (Helenius, Salmelin, Service, & Connolly, 1998; Levelt,
C.L. Ludlow, T. Loucks / Journal of Fluency Disorders 28 (2003) 273–295 275
Praamstra, Meyer, Helenius, & Salmelin, 1998; Numminen, Salmelin, & Hari,
1999).
For example, investigators have examined the dynamic interplay between re-
sponses in different brain regions during single word reading (Salmelin, Helenius,
& Service, 2000; Salmelin, Schnitzler, Schmitz, & Freund, 2000). When neural
events were examined within a 400 ms time period between word presentation and
motor execution, predominant processing occurred in the left hemisphere in both
persons who stutter (PWS) and controls. However, the sequence of activation dif-
fered between groups indicating that the dynamic interplay between brain regions
is altered in persons with life-long stuttering. The normal speakers had earlier
responses in the left inferior region processing prior to left central motor region
activation. The sequence was reversed in the PWS group; these speakers activated
the left central MI region for motor execution before the left inferior region for
articulation programming.
Reduced activations in auditory association regions in PWS were also found
by Fox et al. (2000) and Braun et al. (1997) using PET scanning. This could be
interpreted as being an abnormal suppression of auditory feedback while speaking.
Using MEG, Numminen et al. were able to examine responses to auditory stimuli
during oral reading and found that they were normally suppressed in control sub-
jects by 44–71% in comparison with responses during silent reading (Numminen
et al., 1999). A subsequent study by Curio, found that cortical responses to one’s
own voice transiently activate the right hemisphere around 100 ms after their utter-
ance by a speaker (Curio, Neuloh, Numminen, Jousmaki, & Hari, 2000). However,
on the left side, this was delayed by 11 ms in normal speakers only during speak-
ing and not during listening (Curio et al., 2000). It was suggested that speaking
normally both dampens and delays responses in the auditory cortex in the left
hemisphere. A similar study was conducted in PWS and controls contrasting audi-
tory responses during silent reading, reading aloud and chorus reading (Salmelin
et al., 1998). Responses to auditory stimuli differed during the different conditions
in the PWS. The authors suggested that responses to auditory stimuli were most
altered during self-paced reading in PWS, when an abnormal pattern of greater
auditory suppression occurred on the right and reduced suppression on the left.
Surprisingly, the normal pattern of greater auditory suppression on the left and
reduced suppression on the right, occurred when the subjects were stuttering. The
results implicate different excitatory and inhibitory inter-relationships between
brain regions in normal and PWS groups rather than one particular region being
dysfunctional.
Subtle fine motor deficits can be found in PWS in other motor systems (Borden,
1983; Forster & Webster, 1991, 2001; Webster, 1990). In addition, sensory function
differences have been found in PWS; the effects of sensory deprivation reduces
fluency (Hutchinson & Ringel, 1975) while the ability of PWS to use sensory
feedback is affected for oral movements but not for hand movements (De Nil &
Abbs, 1991; Fucci, Petrosino, Schuster, & Belch, 1991; Petrosino, Fucci, Gorman,
& Harris, 1987). Although differences in sensory motor functioning may affect
other motor systems in some PWS, most often the oral-motor system is selectively
affected and this is most evident during speech.
Symptom occurrence is intermittent, however — fluent speech occurs the vast
majority of the time in PWS, albeit with considerable effort. Stuttering occurs
around 10% of the time, although subjects report they consciously monitor their
speech to prevent disruptions most of the time. The system seems most easily
disrupted when the demands for rapid and dynamic processing increase (Bosshardt,
2002). It may be the functioning of the integrated system that is altered not the
individual components per se.
Some have suggested that left hemisphere dominance for the control of speech/
language is altered in PWS. Neuroimaging studies demonstrate that both the left
and right motor and sensory regions are active in normal speakers during speech
production (Braun et al., 1997). However, WADA testing, where a barbiturate is
infused into the right or left cerebral arterial system, has demonstrated that the
left hemisphere is essential for speech and language expression in most persons
who have not sustained a left hemisphere lesion in early childhood (Rasmussen &
Milner, 1977). Similarly, the occurrence of aphasia following left hemisphere le-
sions is much more frequent than following right hemisphere lesions (Mazzocchi &
Vignolo, 1979). For speech production, rather than language processing, however,
it is unclear to what degree speech production is lateralized (Rasmussen & Milner,
1977). One study used the WADA technique to demonstrate bilateral control of
speech in four persons who stuttered following brain injury (Jones, 1966). Another
study, however, found that speech was disrupted on the right side only in a patient
who had previously had brain injury and aphasia as well as stuttering. The other
persons with idiopathic stuttering, only had speech disruption with amytal infusion
on the left side, similar to normal (Andrews, Quinn, & Sorby, 1972). Similarly, a
study of three PWS without brain injury found all had left hemisphere dominance
for speech on WADA testing (Luessenhop, Boggs, LaBorwit, & Walle, 1973).
There is no evidence to suggest reversed laterality in PWS, rather the data suggest
differences in the functional inter-relationships between brain regions on the right
and left sides during speech and language processing in PWS.
Phonemic expression has been suggested to depend upon intact neural mecha-
nisms in the left insula, based on injury data (Dronkers, 1996) and neuroimaging
in normal speakers (Wise, Greene, Buchel, & Scott, 1999). That is, left insula
functioning is likely involved but must interact with other regions in both the left
and right hemispheres occurs during speech. The evidence thus far suggests that
speech production may have a different degrees of involvement of right hemi-
sphere mechanisms for speech during stuttering (Braun et al., 1997; Fox et al.,
1996, 2000). Wood found inadequate left frontal activation during stuttering using
zenon blood flow measures. This normalized after administration of haloperidol
to induce fluency (Wood, Stump, McKennhan, Sheldon, & Proctor, 1980). Stud-
ies are needed to examine the intricate sequence and timing relationships among
these neural mechanisms during ongoing speech both in normally fluent speakers
and PWS during both fluent and stuttered utterances. As some of the MEG data
suggest, the ability to effect the dynamic interplay between neural mechanisms
may be altered in PWS.
3. Location of brain injury that induces speech dysfluency
A review of the location and types of brain lesions that can induce acquired
stuttering can be informative if one hypothesizes that a particular brain region
may be essential for fluent speech. To test this hypothesis, the studies reporting on
acquired stuttering were reviewed.
Acquired stuttering is qualitatively different from developmental stuttering,
possibly because stuttering during development alters emotional and psycholog-
ical factors associated with speaking. As a result, anxiety, fear and embarrass-
ment may become associated with speech communication in those who have stut-
tered since childhood. Acquired stuttering is different from uncontrolled rapid
festinating syllable repetitions that occur during palilalia (LaPointe & Horner,
1981). Rather, acquired stuttering involves repetitions, vowel prolongations and
occasional blocks (Ludlow, Rosenberg, Salazar, Grafman, & Smutok, 1987). The
symptoms alone cannot be easily differentiated from developmental stuttering (Van
Borsel & Taillieu, 2001). The similarities in the speech symptoms of the develop-
mental and acquired forms, lends credence to the need for analysis of which brain
lesions can induce stuttering in adults.
Early studies of acquired stuttering were case reports that lacked imaging data
and were unable to determine the location and extent of the brain lesions. More re-
cent reports, however, were able to assess the lesion location (Table 1). These lesion
data do not demonstrate that any one brain region is more likely involved in the ac-
quisition of stuttering. Many of the more recent studies, which used neuroimaging,
reported involvement of the basal ganglia, with the putamen being listed most often
(Abe, Yokoyama, & Yorifji, 1992; Andy & Bhatnagar, 1991; Carluer et al., 2000;
Ciabarra, Elkind, Roberts, & Marshall, 2000; Heuer, Sataloff, Mandel, & Travers,
1996; Kono, Hirano, Ueda, & Nakajima, 1998; Lebrun, Leleux, & Retif, 1987;
Leenders et al., 1986; Ludlow et al., 1987; Shibuya, Wakayama, Murahashi, Aoki,
& Ozasa, 1998). A few other studies have reported injuries involving the corpus
callosum (Hagiwara, Takeda, Saito, Shimizu, & Bando, 2000; Soroker, Bar-Israel,
Schechter, & Solzi, 1990; Tsumoto, Nishioka, Nakakita, Hayashi, & Maeshima,
1999). Only a small number of imaging studies suggest that primarily cortical
regions are involved (Bijleveld, Lebrun, & van Dongen, 1994; Franco et al., 2000;
Grant, Biousse, Cook, & Newman, 1999; Turgut, Utku, & Balci, 2002) with most
of these indicating diffuse cortical injury (Mouradian, Paslawski, & Shuaib, 2000;
Rao, 1991). Other older studies do not provide imaging data (Fleet & Heilman,
1985; Helm, Butler, & Benson, 1978; Rosenbek, Messert, Collins, & Wertz, 1978).
On the other hand, studies documenting a cessation of stuttering following brain
injury involve either diffuse lesions (Miller, 1985) or thalamic injury or stimulation
(Andy & Bhatnagar, 1992). One study documented the cessation of stuttering fol-
Table 1
A review of previously reported cases of acquired stuttering following brain lesions and cases of stuttering cessation following brain lesions
278
Author Year Pathology Imaging Number Side Structures History of
stuttering/LH
Turgut 2002 CVA CT 1 Left Parietal No
C.L. Ludlow, T. Loucks / Journal of Fluency Disorders 28 (2003) 273–295

Casado 2000 CVA MRI 1 Left Left precentral — left internal
carotid occlusion
Hagiwara 2000 CVA MRI 1 Right Right corpus callosum — right
anterior artery
Ciabarra 2000 CVA MRI 1 Left Rostromedial infarct
MRI 1 Left Putamen
MRI 1 Left Putamen Left handed
Mouradian 2000 CVA MRI 1 Left Nonspecific white matter changes
Carluer 2000 CVA CT 1 Left Basal ganglia (putamen, caudate
and posterior internal capsule)
Grant 1999 CVA MRI 1 Left Middle cerebral artery
1 Left Temporal lobe Yes
1 Right Parietal Yes
1 Left Occipital Left handed
Tsumoto 1999 CVA MRI 1 Right Cerebral artery — involves
corpus callosum
Kono 1998 CVA CT, MRI 1 Left Striatocapsular infarct to
putamen and caudate
Shibuya 1998 CVA MRI 1 Bilateral Basal ganglia and periventricular
white matter
Heuer 1996 CVA CT, MRI 1 Right Periventricular white matter, left
thalamus, right caudate
1 Bilateral Putamen, caudate right cerebral
artery
1 Left Left temporal, mesial posterior Left handed
thalamus
Bijleveld 1994 CVA 1 Left Frontal and temporal
Abe 1992 CVA 1 Bilateral Midbrain and bilateral medial
thalamus
Andy 1991 Chronic pain Placement of 1 Unclear Mesothalamus
stimulator
Rao 1991 Head injury None 1 Unclear Closed head injury
C.L. Ludlow, T. Loucks / Journal of Fluency Disorders 28 (2003) 273–295

Soroker 1990 CVA None 1 Right Callosum
Ludlow 1987 Missile wounds CT 10 5 right, 4 left, Internal and external capsules, 4/14 with history
1 bilateral frontal WM, striatum of stuttering
Lebrun 1987 CVA CT 1 Right Parietal, subcortical extent
Leenders 1986 CVA CT, MRI 1 Left Brainstem — thalamic. Left
striatum
Fleet 1985 Arteriogram 1 Right Internal carotid artery
Rosenbek 1978 CVA None 7 5 left, 1 right, One had previous stuttering
1 bilateral
Helm 1978 CVA or HI None 10 8 bilateral 6 multiple CVAs, 4 head trauma
Cessation of stuttering
Muroi 1999 CVA MRI 1 Bilateral Medial thalamus Cessation of
stuttering
Andy 1992 Chronic pain None — placement 4 Unclear Mesothalamic stimulation Cessation of
of stimulator stuttering
Miller 1985 Multiple sclerosis None 2 Unclear Cerebellar dysfunction Cessation of
stuttering
Jones 1966 Brain tumor WADA test — 1 Left Frontal brain tumor since LH — cessation
bilateral speech childhood — bilateral speech of stuttering
Subarachnoid WADA test — 1 Right Right cerebral artery — bilateral Cessation of
hemorrhage bilateral speech speech stuttering
Subarachnoid WADA test — 1 Left Left anterior communicating LH — cessation
hemorrhage bilateral speech artery of stuttering
Subarachnoid WADA test — 1 Left Left cerebral artery LH — cessation
hemorrhage bilateral speech of stuttering
279
lowing unilateral brain injury in four persons who had previously stuttering since
childhood and had bilateral speech representation based on the WADA test (Jones,
1966).
The articles listed in Table 1 demonstrated some left hemispheric preference
for inducing stuttering: 47% were left sided lesions, 26% were right and 26% were
bilateral. Of those with imaging findings reported, 75% involved subcortical re-
gions (basal ganglia, thalamus, internal capsule and corpus callosum). Similar to
developmental stuttering, there was a 5:3 male to female ratio when sex was ex-
amined across these studies. Further, a normal handedness distribution was found;
80% were right handed and 19% were left handed. Few authors reported whether
patients had previously stuttered during childhood; however of 57 cases, 14% re-
ported childhood stuttering. This is a higher frequency than the 1% incidence of
stuttering in adults. Apparently, those who recovered from childhood stuttering
have a greater vulnerability for acquired stuttering after brain lesions.
The only conclusion that can be made from these studies are that the lesions
associated with acquired stuttering rarely involve the primary speech and lan-
guage regions in the left hemisphere (Broca’s area, the temporal planum, insula
or Wernicke’s area). When these regions are involved, patients usually exhibit
aphasia, which might mask stuttering symptoms, however, such patients do not
exhibit stuttering when they recover (Ludlow et al., 1986). Therefore, the lesions
leading to acquired stuttering seem to be those that impinge upon structures that
support and modulate rapid communication between brain regions such as the
corpus callosum, or areas that exert influence on multiple brain regions such as
the basal ganglia and thalamus. The lesions in either the corpus callosum or thala-
mus could interfere with rapid communication of distributed areas during speech
production. On the other hand, they were not disconnection lesions within the
speech and language system in the left hemisphere which result in different types
of aphasic syndromes (Geschwind, 1965a, 1965b). Rather, these lesions disturb
rapid coordinated functioning of the brain networks. Acquired stuttering did not
occur when brain regions involved in speech and language functions were irrevo-
cably damaged; rather it occurred when the speech and language areas were not
able to inter-relate with other brain regions in a rapid dynamic fashion.
Stuttering may reflect a poorly coordinated speech system possibly because
of deficient development of white matter tracts (Sommer, Koch, Paulus, Weiller,
& Buchel, 2002) or reduced neural pruning (Foundas, Bollich, Corey, Hurley, &
Heilman, 2001). The former was further supported by the recent results of Som-
mer et al., who found higher thresholds for hand muscle responses to transcranial
magnetic stimulation over the motor cortex in stuttering adults (Sommer, Wischer,
Tergau, & Paulus, 2003). Stuttering may reflect an instability or loss of control
in brain function rather than a loss of function — which makes stuttering simi-
lar to some other motor control disorders such as tremor, dystonia or Gilles de la
Tourette’s syndrome (TS). To expand this view, a review of the some of the similar-
ities and differences between stuttering and other speech motor control disorders
is helpful.
4. The similarity and differences between stuttering and other speech

motor control disorders
On first approximation, the phenomenology of stuttering seems commensurate

with a neurologically based developmental motor control disorder (Brin, Blitzer, &
Stewart, 1998; Kiziltan & Akalin, 1996). If the sensorimotor differences identified
in stuttering have more similarities than differences relative to other speech motor
control disorders, then this initial approximation is supported.
Speech production takes place during human communication, except in speech
science laboratories where subjects are tested while producing meaningless phrases
modeled by the tester. Such well controlled speech research tasks rarely elicit
stuttering — stuttering is more frequent when subjects are required to formulate
meaningful communication (Ratner, Gawronski, & Rice, 1964; Ratner & Sih,
1987). This augmentation of symptoms during communication is more pronounced
in stuttering, but is a common feature of most speech and voice motor control
disorders (Caligiuri, 1989; Sarno, 1968). In dysarthria and voice disorders, patients
are often able to produce the target behavior in the clinical setting when attention
is focused on production. After they leave the clinic, however, they tend to revert to
impaired performance during conversation with others — a phenomenon referred
to as carry-over (Klaff, 1976). In TS, patients can control symptoms for short
periods, only to have them emerge in a more frequent pattern when they are no
longer monitoring or controlling them.
Stuttering is a task specific disorder — that is, oral-motor dysfunction becomes
apparent only during speech and not during humming, singing or chewing. In spas-
modic dysphonia (SD), which is a laryngeal dystonia, the voice disruptions are most
manifest during speech and much less evident during simple vowel prolongation
(Sapienza, Murry, & Brown, 1998) and singing (Bloch, Hirano, & Gould, 1985).
In TS, symptoms occur at rest but are increased by 30% during speech (Ludlow,
1993). The separation mentioned earlier, between non-meaningful speech produc-
tion which is usually symptom free, and linguistic communication with enhanced
stuttering (Perkins, Kent, & Curlee, 1991) is also a task dependent attribute. Task
related differences also occur in oral-mandibular dystonia where some patients may
only have oral-motor muscle abnormalities during speech but not during chewing,
while others only have chewing affected with no oral-motor abnormalities during
speech (Rosenbaum & Jankovic, 1988).
The difference in the occurrence of symptoms during speech communication
and emotional expression is also task related. Laughter and crying are usually nor-
mal in both PWS and persons with SD (Bloch et al., 1985). In SD, this difference
previously led to the assumption that the disorder was psychogenic. Now this dif-
ference is understood as evidence of different vocalization systems being present
in human and non-human primates. Singing is thought to involve different brain
regions from speech, particularly in the right hemisphere (Riecker, Ackermann,
Wildgruber, Dogil, & Grodd, 2000) and simple vocalization and emotional ex-
pression may involve the cingulate and periaquaductal grey (Jurgens, 2002). On
the other hand, speech communication involves both cortical and subcortical
systems.
Stuttering is more frequent when central processing demands increase with
greater speech complexity or dual processing tasks (Bosshardt, 2002; Hall,
Yamashita, & Aram, 1993; Starkweather, 2002). Similarly, in SD, motor function
and electromyographic abnormalities are more impaired on complex processing
tasks (Schaefer et al., 1992).
Both disorders are focal, that is they involve oral-motor or laryngeal musculature
but not other motor systems. Reich, for example, conducted similar studies in both
disorders, comparing laryngeal and manual reaction times with similar results, the
laryngeal or phonatory systems were affected while the manual systems were not
(Reich & Till, 1983; Reich, Till, & Goldsmith, 1981).
One difference between these disorders, of course, is the age of onset. Given this
difference it is surprising that both groups have similar reactions to their speech
disorder. Persons with SD, which onsets in adulthood, develop an adverse reaction
to telephone use, become socially isolated and often develop a reactive depres-
sion (Cannito, 1991) which resolves with treatment (Murry, Cannito, & Woodson,
1994). Developmental stuttering often involves the development of similar fear
and avoidance reactions to the telephone and feelings of social isolation (Miller &
Watson, 1992). Persons with either disorders may develop a social anxiety disorder
secondary to their voice and speech impairments (Moutier & Stein, 1999).
The task specific attributes of stuttering and SD implicate two possible selective
aspects of these disorders. First, they only appear during speech sound production
which has more rapid and precise motor control demands on vocal tract motor
control (Ludlow & Lou, 1996). Second they implicate that one system is affected,
that required for speech production during communication and language, while an-
other is not. The vocal spasms of SD and the repetitions, prolongations and pauses
in stuttering point to the intermittent nature of both disorders during speech pro-
duction. The intermittent nature of these disorders support a serious consideration
of whether the central control abnormalities may be similar.
Another disorder with intermittent vocal symptom occurrence is Tourette’s
syndrome, a developmental disorder with onset most often between 5 and 12
years of age. This disorder involves multiple and one or more vocal tics occur-
ring either many times a day or intermittently in a year, the tic characteristics
can change over time, have onset before 21 years and are idiopathic, that is, not
exclusively due to psychoactive substance intoxication or due to known central
nervous system disease (Diagnostic and statistical manual of mental disorders,
1987). Speech and vocal tics occur at rest in TS, are exacerbated during speech
(Ludlow, 1993; Ludlow, Polinsky, Caine, Bassich, & Ebert, 1982) but occur
primarily at the beginning of speech or during speech pauses (Frank, 1978;
Martindale, 1976, 1977). No differences in tic production occur with delayed audi-
tory feedback or white noise or reduced speaking rate, which differs from stuttering
symptom characteristics (Ludlow, 1993). Different authors have noted, however,
that a high proportion of persons affected with TS report stuttered as a child (45%
reported developmental stuttering in one report, Ludlow, 1993), and an associa-

tion between stuttering and TS in families was reported by one group (Comings
& Comings, 1994; Comings, Comings, & Knell, 1989; Comings et al., 1996), al-
though not supported by others (Pauls, Leckman, & Cohen, 1993). Some intriguing
similarities, however, are that both disorders are benefited by dopamine receptor
blockade (Kossoff & Singer, 2001; Ludlow & Braun, 1993), may be genetically
related, wax and wane in severity, start in childhood, and spontaneously remit later
in a large proportion of cases. Recent functional neuroimaging has demonstrated
that TS involves aberrant activity in the precentral gyrus, insula, anterior cingulate
and basal ganglia coupled with hypoactivity in the sensorimotor cortices (Stern
et al., 2000). Increased activity in some of the same regions have been associated
with the production of stuttering (Braun et al., 1997; Fox et al., 2000). Several
TS patients report that tics are preceded by premonitions or urges to tics. Oth-
ers emphasize that sensations often precede tics and that the tic is a response
to a sensory experience. In stuttering, similar premonitions can occur prior to
dysfluencies.
TS, however, is not a task specific disorder or focal to the speech musculature
as is the case for both SD and stuttering, although vocal and speech tics are a
necessary part of the syndrome. Therefore, there are more similarities between
stuttering and SD than between stuttering and TS in motor symptoms.
4.1. Sensory deviations
A distinctive attribute of the focal dystonias are sensory anomalies that involve
sensory tricks, deviant reflexes, sensory perception differences and abnormal sen-
sory evoked potentials (Hallett, 1995). Sensory tricks are used by individuals with
focal dystonias to control symptoms, such as, touching the face in Meige syndrome
or chewing tooth-picks in oromandibular dystonia (Rosenbaum & Jankovic, 1988).
In SD, a similar reduction in symptoms can occur during fiberoptic nasolaryn-
goscopy, presumably due to altered sensation during placement of the nasolaryn-
goscope in the oropharynx. Compensatory speech patterns, such as whispering,
that are often observed clinically (Bloch et al., 1985) also alter sensory feedback.
We have studied laryngeal closure reflexes in the thyroarytenoid muscle in re-
sponse to electrical stimulation of the laryngeal afferents contained in the superior
laryngeal nerve in normal speakers and persons with SD. When paired electrical
stimuli are presented at less than 1 s intervals for conditioning the late R2 responses
(>60 ms latency) are normally suppressed reflecting central inhibitory processes
modulating these responses. Conditioning abnormalities of the R2 response of the
laryngeal adductor reflex have been found in both the adductor and abductor types
of SD suggesting an abnormality in central suppression of muscle responses to
sensory feedback (Deleyiannis, Gillespie, Bielamowicz, Yamashita, & Ludlow,
1999; Ludlow, Schulz, Yamashita, & Deleyiannis, 1995). Decreased or altered af-
ferent feedback reduce spasmodic bursts in some of the dystonias (Kaji, Rothwell,
et al., 1995; Yoshida et al., 1998).
As mentioned earlier, a number of studies point to corresponding sensory func-

tion differences in stuttering. Psychophysical studies indicate PWS have higher
perceptual somatosensory thresholds for minimal movements of the jaw, lower
lip and tongue and lingual vibrotactile stimuli. Persons who stutter also show de-
viant kinesthetic perceptions of jaw position on movement accuracy tasks (De Nil
& Abbs, 1991). Certain differences relative to SD are noted though. A bilateral
blockade of oral sensation was associated with increases in the frequency of stutter-
ing symptoms (Hutchinson & Ringel, 1975), unlike the effects of lidocaine in some
of the dystonias (Kaji, Kohara, et al., 1995). Although an influential hypothesis
suggested exaggerated reflex gains could lead to stuttering (Zimmermann, Smith,
& Hanley, 1981), evidence for marked oral reflex deviations have not been found,
although labial reflex gains may be slightly altered in PWS (McClean, 1987).
The observations of so-called secondary or compensatory behaviors in stutter-
ing show a broad similarity to the sensory tricks and compensatory speech adjust-
ments used by persons with focal dystonias (Kiziltan & Akalin, 1996; Mulligan,
Anderson, Jones, Williams, & Donaldson, 2001). Reductions in stuttering symp-
toms are associated with altered speech patterns (whisper, choral speech) and un-
usual oral gestures or bodily movements. Such movement changes potentially alter
auditory and somatosensory inputs in turn helping to avoid or suppress stuttering
— and could be interpreted as sensory tricks.
The most profound sensory effects, however, are those of auditory feedback
manipulations (delayed auditory feedback, masking, etc.) that significantly
suppress stuttering symptoms. The role of auditory feedback has also had a partic-
ular role in speech fluency: the paradoxical effects of chorus reading and delayed
or altered feedback is pronounced in this disorder (Adams & Ramig, 1980; Stager,
Denman, & Ludlow, 1997), although also present in dysarthria in Parkinsonism
(Hanson & Metter, 1983). However, extended exposure to altered auditory feed-
back leads to less dramatic effects (Armson & Stuart, 1998) and it may not be the
auditory modality per se but rather any significant change in the speaking con-
text (Kalinowski, Stuart, Rastatter, Snyder, & Dayalu, 2000) that can alter fluency.
One small study found no effect of white noise of delayed auditory feedback on
symptom occurrence in TS (Ludlow, Nauton, & Bassich, 1984).
Even if sensory abnormalities in either the larynx or orofacial structures are
identified in either disorder, the role of sensory abnormalities in these disorders
still requires elucidation. It has been long recognized that suppression of sensory
information that is possibly redundant or that could interfere with ongoing move-
ment is possibly just as critical for the coordination of movement as the receipt of
sensory information. Inappropriate or a lack of inhibition in SD or stuttering could
indeed be a central factor in the emergence of vocal spasm or stuttering events, as is
suggested for SD by the reduction in R2 conditioning. Studies of abnormal sensory
inhibition of brain responses to afferent feedback in stuttering are an avenue that
can be addressed with rapid neurophysiological recording using MEG as has been
done for auditory feedback (Salmelin, Helenius, et al., 2000; Salmelin, Schnitzler,
et al., 2000).
4.2. Muscle interference
Earlier ideas about the physiological basis for dysfluencies in both disorders in-
volved speculation that tonically increased activity in the laryngeal muscles caused
speech disruptions in SD and stuttering. In the adductor type of SD, Nash and
Ludlow (1996) identified intermittent increases in thyroarytenoid activity during
voice breaks, but that the overall level of muscle activity was not abnormal (Van
Pelt, udlow, & Smith, 1994). Thus, spasmodic bursts in the thyroarytenoid mus-
cles intruded upon otherwise unremarkable muscle recruitment (Nash & Ludlow,
1996). Muscle bursts in the abductor type of SD are more variable across subjects
(Cyrus, Bielamowicz, Evans, & Ludlow, 2001), but again tonically elevated mus-
cle tone has not been observed (Van Pelt et al., 1994). The mechanism involved in
muscle bursts during voice breaks may arise from deficient suppression of laryn-
geal sensorimotor reflexes in both SD types. In SD, abnormal central modulation
of brain stem mechanisms may result in reduced suppression of laryngeal reflexes
in response to the sensory feedback due to speech and voice production, in an
otherwise normal neural circuit for phonation.
In stuttering, evidence for elevated tonic activity in the laryngeal or orofacial
muscles has not been found during speech disruptions (Smith et al., 1993; Smith,
Denny, Shaffer, Kelly, & Hirano, 1996). Tonic co-contraction of the laryngeal mus-
cles during stuttering was first reported by Freeman (Freeman & Ushijima, 1978),
but the study was flawed, because of the lack of a control group. Subsequent con-
trolled studies of laryngeal muscle and orofacial muscles have not found tonic
over-activity or abnormal co-contraction during fluent speech or dysfluencies in
PWS (Smith et al., 1996). Instead, approximately 50% of adults and teens who
stutter display high frequency oscillations (6–15 Hz range) in the orofacial and
laryngeal muscles during stuttering dysfluencies but not during fluent speech. The
oscillations occurred simultaneously in multiple vocal tract muscles and have been
likened to tremorogenic activity (Smith et al., 1993). The 50% incidence of the
oscillations prevents them from being considered characteristic of stuttering and
distances stuttering from SD, which shows a nearly universal incidence for burst-
ing abnormalities in a limited set of muscles during speech breaks. Finer resolution
analyses of muscle activity during stuttering may identify other aberrations in mus-
cle activity, but it remains likely that stuttering dysfluencies may involve normal
muscle electromyographic amplitudes and spectral characteristics. Although mus-
cle activity during a dysfluency is not characterized by spasms, tremor or excessive
co-contraction, questions remain whether the coordination of muscle activation is
aberrant or if there is an absence of normal muscle inhibition during stuttering.
Increased cortical excitability in motor regions has been implicated in both
SD and stuttering by functional neuroimaging during symptom production (Braun
et al., 1997; Fox et al., 1996, 2000; Hirano et al., 2001). Whether cortical ex-
citability is due to decreased cortical inhibition can be examined using transcra-
nial magnetic stimulation using a conditioning paradigm. First, motor thresholds
are determined for eliciting a motor evoked potential (MEP) in a hand muscle in
response to cortical stimulation in the primary motor area. Next, cortical inhibition
can be assessed using a conditioning paradigm where a sub-threshold conditioning
stimulus (at 90% of motor threshold amplitude) precedes a supra-threshold test
stimulus at time intervals between 1 and 30 ms. The degree to which the MEP
response to the test stimulus is suppressed relative to an MEP to an unconditioned
stimulus of the same strength is measured (Kujirai et al., 1993). Increased exci-
tation of hand muscle responses using this paradigm was found in various focal
dystonias such as writer cramp and blepharospasm (Sommer, Ruge, et al., 2002).
In a recent study, using the same conditioning paradigm to study hand muscle
response inhibition, no abnormalities in inhibition were found in PWS (Sommer
et al., 2003). The PWS group, however, had significantly higher motor thresh-
olds for eliciting hand muscle responses than the controls, which was unexpected.
These findings may suggest a different pathophysiology in stuttering, that is, a
reduced cortico-spinal tract excitability to hand muscles in PWS. Further study
is needed to examine whether similar findings occur in SD. Also, conditioning
studies of cortical excitability for oral and laryngeal musculature is needed in both
SD and TS.
Because stuttering dysfluencies are not specific to a small set of muscles, this
may explain why botulinum toxin injections have not and will not likely be appro-
priate treatment for stuttering (Stager & Ludlow, 1994) even though it is clearly
the most effective treatment to date for SD (Truong, Rontal, Rolnick, Aronson, &
Mistura, 1991). Botulinum toxin injection, however, suppresses muscle spasms by
denervating both the muscle fibers and muscle spindles. Current behavioral treat-
ments for stuttering may also predominantly involve muscle suppression. Treat-
ments that instead target the central mechanisms may be most effective in both
disorders, because any abnormal muscle activity in either disorder is secondary to
the central pathological mechanisms.
4.3. Central abnormalities
Along with arguments for deviancies in sensori-motor processing and muscle

activation in PWS and SD, abnormalities in cortical and/or subcortical processing
are thought to be present in both disorders. Only a few studies of brain function
have been conducted in either disorder.
A case study of a person with SD using positron emission tomography (H2 15 O
PET) indicated reduced regional cerebral blood flow (RCBF) responses in the
supplementary motor area (SMA) and increased RCBF in the left superior tem-
poral gyrus during phonation relative to six control subjects (Hirano et al., 2001).
Findings for a single subject are difficult to interpret however, due to the high vari-
ability of RCBF both between participants and across tasks. Studies in other forms
of dystonia have shown deficient central activation in response to sensory feed-
back (Tempel & Perlmutter, 1990, 1993). Similarly, patterns of hyperactivation and
hypoactivation have been found in PWS. Hypoactivation of the left post-central
sensory and auditory association regions were found in PWS during dysfluency
evoking tasks by Wu et al. (1995), Fox et al. (1996, 2000), and Braun et al. (1997).
At the same time increased activation in premotor and motor areas have been found
in both stuttering and dystonia (Braun et al., 1997; Odergren, Stone-Elander, &
Ingvar, 1998). Firm conclusions regarding similar patterns of brain dysfunction
in the two disorders cannot be made given the limited data, particularly for SD.
However, the corresponding patterns of sensory hypoactivation and frontal motor
and premotor hyperactivation make a potential link between the disorders more
compelling.
4.4. Basal ganglia abnormalities
Basal ganglia dysfunction has been viewed as the most probable dysfunctional
region in primary dystonias, in which the failure of the basal ganglia circuitry to in-
hibit inappropriate cortical motor control regions may lead to pathological muscle
activation and dystonic posturing (Galardi et al., 1996). Given that basal ganglia
output modulates cortical motor areas, the logic behind hypotheses of basal ganglia
dysfunction in dystonia is attractive. The neuroimaging studies of stuttering also
point to atypical basal ganglia activation or abnormal activity in areas receiving
basal ganglia output. Wu et al. (1995) reported hypoactivation in the left caudate
nucleus during both fluency and dysfluency evoking tasks. In the Braun et al. study
(Braun et al., 1997), PWS showed higher activity in the right caudate nucleus and
generally lower activation in SMA compared to controls in both the dysfluent
and fluent conditions. Consequently, the still limited evidence from neuroimag-
ing indicates atypical activity in the basal ganglia or in areas receiving efferent
output from basal ganglia nuclei. The brain lesion data on acquired stuttering re-
viewed earlier, suggest that basal ganglia dysfunction can induce stuttering in fluent
adults.
To date, the focal dystonias have not been found to be responsive to neurophar-
macological intervention (Brin et al., 1998) and stuttering is only benefited by
dopamine receptor blockade although the side effects usually outweigh the ben-
efits (Ludlow & Braun, 1993). Paroxetine has been reported to have serious side
effects (Bloch, Stager, Braun, & Rubinow, 1995) and risperidone has fewer side ef-
fects but limited long term benefits (Lee et al., 2001; Maguire et al., 1999; Maguire,
Riley, Franklin, & Gottschalk, 2000).
4.5. Vulnerable systems
Stuttering and SD are both idiopathic disorders; that is they are not normally
secondary to any know disease or disorder but emerge spontaneously, one during
development and the other during adulthood. Both disorders can emerge during
stressful events, not because stress is a cause of the disorder but rather because the
speech motor system in such persons may be more vulnerable to breakdown when
stress is increased. No studies have addressed the rate of co-occurrence of these
disorders in families.
Our consideration of the similarities and differences between stuttering and

other speech motor control disorders such as SD, is aimed at stimulating new
avenues for hypothesis-driven research into the mechanisms of stuttering. Sensory
processing irregularities in stuttering that are similar to focal dystonias could be
investigated using whole head magnetoencephalography to further assess whether
the time courses, amplitudes and source locations of oral somatosensory and/or
auditory evoked potentials are deviant in stuttering. Application of functional MRI
(fMRI) to neurocognitive and neuromotor processes in stuttering (and SD) have
barely been initiated, but the success of fMRI in understanding brain activation
for such processes indicates it holds promise for understanding central processes
in stuttering. The possibility that cortical pryramidal tract excitation is affected in
stuttering (Sommer et al., 2003) needs to be investigated further. Certainly, PET
techniques could be used to measure neurotransmitter uptake and to assess basal
ganglia function, techniques which have already added improved understanding
of the pathogenesis in Parkinson’s disease (Ito et al., 2002). Integrating these
research questions with good data on the simultaneous activity in different brain
mechanisms should help to parse out the dynamic inter-relationships and how these
differ in stuttering both between tasks and from normal.
The major difference between stuttering and focal dystonia is the age of on-
set. The period of vulnerability for developing stuttering is between 2 years of
age and puberty. The neurobiology of development may underlie the bases for
the emergence of stuttering in childhood. Developmental neurobiology involves
two overall processes, the initial growth stages of cellular proliferation, migra-
tion, differentiation and synaptogenesis which occur in the prenatal and early
post-natal periods (Purves, 1994) and the later stages of selective refinement.
Early childhood, the period of vulnerability for the development of stuttering,
may include processes involved in refinement of the neurological system. Re-
duction and refinement occur through dendritic pruning, programmed cell death
and selective enhancement of networks of synaptic connections (Purves, 1994).
Reduction and refinement in neural processes may be essential for the develop-
ment of normal speech motor control based in part, on activity and use. That is,
as some synaptic connections are enhanced through use, others are lost through
inactivity, shaping the emergence of efficient circuitry for speech function within
the central nervous system. Although little information is available on the refine-
ment process within the speech motor control system during childhood, it can
be assumed that it follows the same neurodevelopmental processes as the rest of
the central nervous system. The recent finding of increased size in the right and
left planum temporali in stuttering adults and additional gyri in perisylvian re-
gion compared to normal (Foundas et al., 2001) may suggest abnormal pruning.
On the other hand, reduced white matter tracts in central areas (Sommer, Koch,
et al., 2002) might suggest abnormal growth and refinement processes during
development.
In summary, the evidence to date suggests that stuttering is a neurodevelop-
mental motor control disorder. It has some intriguing similarities to other motor
control disorders, the focal dystonias, in particular. This suggests that conceptual
frameworks based on the dynamic interplay between different components of the
motor control system and its interface with language processing can be helpful
for the study of the pathophysiology of both disorders. Although the etiologies
are most likely quite different, the functional abnormalities appear to be related
and investigations into the rapid dynamic inhibitory and excitatory processes for
speech production may be beneficial to understanding both disorders.
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CONTINUING EDUCATION
Stuttering: a dynamic motor control disorder
QUESTIONS
1. The brain function abnormalities implicated in stuttering are:

a. Right language dominance
b. Left hemisphere injury
c. Basal ganglia disease
d. Abnormalities in the function of the neural network for speech
2. Brain injuries which cause stuttering in adults involve:
a. Lesions only in Broca’s area
b. Lesions only in Wernicke’s area
c. Lesions only in the basal ganglia
d. Lesions outside Broca’s and Wernicke’s area
3. The similarities between stuttering and dystonias are:
a. Both are task specific and involve emotional expression
b. Both are task specific, focal and intermittent
c. Both are affected by auditory feedback
d. Both affect other disorders besides speech
4. Muscle activity in both stuttering and spasmodic dysphonia:
a. Is abnormal only intermittently in both disorders
b. Is constantly too high in spasmodic dysphonia but not in stuttering
c. Is constantly too high in stuttering but not in spasmodic dysphonia
d. Is normal all of the time in both disorders
5. Neurophysiological studies of persons who stutter indicates that stuttering in-
volves:
a. Language abnormalities
b. Hearing abnormalities
c. Sensory loss
d. None of the above

Stuttering A Dynamic Motor Control Disorder

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Journal of Fluency Disorders

Stuttering: a dynamic motor control disorder

Received 22 July 2003; accepted 29 July 2003

Keywords: Brain lesions; Dystonia; Task specific; Spasmodic dysphonia

∗Corresponding author. Tel.: +1-301-496-9366; fax: +1-301-480-0803.

Our purpose is to identify whether particular neural mechanisms are implicated

1. Recent evidence on the rapid interplay between multiple systems during

3. Location of brain injury that induces speech dysfluency

C.L. Ludlow, T. Loucks / Journal of Fluency Disorders 28 (2003) 273–295

C.L. Ludlow, T. Loucks / Journal of Fluency Disorders 28 (2003) 273–295

4. The similarity and differences between stuttering and other speech

On first approximation, the phenomenology of stuttering seems commensurate

reported developmental stuttering in one report, Ludlow, 1993), and an associa-

4.1. Sensory deviations

As mentioned earlier, a number of studies point to corresponding sensory func-

4.2. Muscle interference

4.3. Central abnormalities

Along with arguments for deviancies in sensori-motor processing and muscle

4.4. Basal ganglia abnormalities

4.5. Vulnerable systems

Our consideration of the similarities and differences between stuttering and

Stuttering: a dynamic motor control disorder

1. The brain function abnormalities implicated in stuttering are:

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