Journal of Neurolinguistics 24 (2011) 383–396

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jneurol ing

Revisiting the acquired neurogenic stuttering in the lightof developmental stuttering

Gopee Krishnan*, Shivani Tiwari 1

Dept. of Speech and Hearing, Manipal College of Allied Health Sciences, Manipal University, Manipal, Karnataka, India – 576 104

a r t i c l e i n f o

Article history:Received 1 October 2010Received in revised form 5 January 2011Accepted 7 January 2011

Keywords:StutteringDysfluencyFluency-enhancing conditionMasked auditory feedbackAdaptation effectBasal ganglia

* Corresponding author. Neuro-CommunicationAllied Health Sciences, Manipal University, Manipal645 9815; fax: þ91 820 2571915 (office).

E-mail address: brain.language.krishnan@gmail1 Fax: þ91 820 2571915 (office).

0911-6044/$ – see front matter � 2011 Elsevier Ltdoi:10.1016/j.jneuroling.2011.01.001

a b s t r a c t

The neural underpinnings of acquired neurogenic stuttering (ANS)remain largely speculative owing to the multitude of etiologies andcerebral substrates implicated with this fluency disorder. System-atic investigations of ANS under various fluency-enhancingconditions have begun only in the recent past and these studies areindicative of the heterogeneous nature of the disorder. In thiscontext, we present the case of a subject with ANS who exhibitedmarked reduction in dysfluencies under masked auditory feedback(MAF), singing, and pacing (speech therapy). However, the adap-tation effect was absent in our subject. By explaining these featuresin the light of recent explanatory hypotheses derived from devel-opmental stuttering (DS), we highlight on the possible similarity inthe neural underpinnings of ANS and DS.

� 2011 Elsevier Ltd. All rights reserved.

1. Introduction

Although acquired neurogenic stuttering (ANS) has been reported for more than 100 years, theunderlying mechanisms of dysfluent speech in this disorder remain largely speculative (Lundgren,Helm-Estabrooks, & Klein, 2010). For instance, with the exception of occipital lobe, ANS has beenassociated with damage to virtually all lobes of the hemispheres (Lundgren et al., 2010), corpus cal-losum (Hamano et al., 2005), brainstem (Balasubramanian, Max, Van Borsel, Rayca, & Richardson,

Disorders Unit (NCDU), Dept. of Speech and Hearing, Manipal College of, Karnataka, India – 576 104. Tel.: þ91 820 2922748 (office), mobile: þ91 903

.com (G. Krishnan), tiwarishivani.2009@gmail.com (S. Tiwari).

d. All rights reserved.

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2003), and cerebellum (Tani & Sakai, 2010a). Further, ANS has also been implicated with severalneurological etiologies such as stroke (Grant, Biousse, Cook, & Newman, 1999; Jokel, De Nil, & Sharpe,2007), traumatic brain injury (Helm-Estabrooks & Hotz, 1998; Lebrun, Bijleveld, & Rousseau, 1990),seizure disorder (Sechi, Cocco, D’Onofrio, Deriu, & Rosati, 2006), encephalitis (Chen & Peng, 1993),Parkinson’s syndrome (Goberman, Blomgren, & Metzger, 2010), and dementias (Quinn & Andrews,1977; Rosenbek, McNeil, Lemme, Prescott, & Alfrey, 1978). Despite these heterogeneities in etiologiesand the underlying neuroanatomical substrates, a consensus on the salient features of ANS has beenarrived at, quite surprisingly (for a recent review on the salient features of ANS, readers are directed toLundgren et al., 2010). In this context, we present the findings from a subject who exhibited certainriveting features discordant with the salient features of ANS. Before proceeding to the presentation ofour subject, a brief review of studies pertaining to the fluency-enhancing conditions in ANS is pre-sented. Further, we also review the recent and relevant functional neuroimaging studies contributingto the current explanatory hypotheses of dysfluent speech.

1.1. Fluency-enhancing conditions

The destructive effects of stuttering on communication can be dramatically reduced under certainfluency-enhancing conditions (e.gs., adaptation effect, singing, chorus/unison reading, and altered [i.e.,delayed, frequency-shifted, or masked] auditory feedback). However, systematic investigations of ANSunder these conditions began only recently (Van Borsel, Drummond, & Pereira, 2010). In the followingsection, we briefly review some of the fluency-enhancing conditions with special focus on ANS.

1.1.1. Adaptation effectThe adaptation effect refers to the reduction in dysfluency with successive readings of the same text

(Johnson & Knott, 1937). The absence of this effect has been considered as a differential feature of ANSfromDS (Culatta & Leeper, 1989–1990). However, recent investigations have shown that the adaptationeffect is highly variable in people with ANS. For instance, in a survey of speech-language pathologists,19% of 52 clinicians reported to have observed adaptation effect, disproving the conventional belief thatthis effect is absent in ANS (Theys, van Wieringen, & De Nil, 2008). Recently, Tani and Sakai (2010b)reported of positive adaptation effect in a cohort of five subjects with ANS. However, the adaptationeffect varied considerably among their subjects and it ranged from 11.1% to 66.7%. Yet another recentstudy (Balasubramanian, Cronin, & Max, 2010), on the other hand, failed to observe any significantadaptation effect in two subjects with ANS, thus adding to the variability of this effect in ANS.

In the literature pertaining to DS, several hypotheses have been proposed to explain the adaptationeffect. For instance, the research on speech motor control has shown that the basal ganglia provide theinternal timing cues necessary for the to-be-produced movements (Max, Guenther, Gracco, Ghosh, &Wallace, 2004). Alm (2004) opined that the practice effect associated with the repeated readingsimproves the basal ganglia timing cues, leading to the reduction of dysfluencies. Max et al. (Max &Baldwin, 2010; Max, Caruso, & Vandevenne, 1997) emphasized the role of motor learning in adapta-tion effect. Max and Baldwin (2010) observed that with subsequent readings spaced two and 24 h, thetrained material exhibited retention of fluency, whereas, the untrained material failed to show anyvariation in dysfluencies. In DS, the generally observed positive adaptation effect is, therefore, attrib-uted to the facilitation of the BG timing cues. In accordance with this proposal, the absence of adap-tation effect reported in ANS population may, therefore, be attributed to the structural and/orfunctional involvement of the BG circuit following the brain damage. On the other hand, the presenceof adaptation effect in ANS is contrary to this hypothesis and its presence and variability warrant moreinvestigations (see Discussion).

1.1.2. SingingSinging is an intriguing task that offers rapid reduction in dysfluencies in DS. It involves the

production of musical tones by means of the voice (Encyclopedia Britannica, 2003) and it consists ofelements such as rhythm and melody. Singing, in opposition to speaking, has been claimed to includedistinct neural areas. For instance, Jeffries, Fritz, and Braun (2003) found activations mainly in the lefthemisphere while speaking, whereas, activations were predominant in the right hemisphere while

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singing. The observation that speaking, but not singing, revealed increased activation in the basalganglia motor circuit (left dorsal putamen) shows that the former task requires timing cues from theBG system, whereas, singing is based on a different strategy of syllable timings, mainly involving theright hemisphere. This difference between speaking and singing is well-documented in the literature(e.g., Yamada & Homma, 2007). In yet another study, Özdemir, Norton, and Schlaug (2006) reportedthat singing, compared to speaking, showed activations in the mid-portion of the superior temporalgyrus as well as in the most inferior and middle portions of the primary sensorimotor cortex of theright hemisphere. It may, therefore, be assumed that during singing, the internal representation of therhythm provides internal timing cues for the initiation of each syllable in a manner similar to theexternal timing cues provided by a metronome. The elimination of stuttering while singing in mostpersons who stutter (PWS) could, therefore, indicate the dysfunctional timing associated with thestutter speech.

In ANS, singing has shown variable results in dysfluency reduction. In Theys et al.’s (2008) survey,among 28 stroke patients with ANS, majority (N ¼ 19) showed stuttering during multiple speech taskssuch as reading, singing, and automatic speech compared to nine subjects with dysfluencies onlyduring spontaneous speech task. In the same study, among nine other subjects with ANS arising fromnon-stroke etiologies such as brain surgery, epilepsy, encephalitis, and medication, five stuttered onlyduring spontaneous speech.

1.1.3. Choral speechSeveral authors have reported that choral (or unison) speech brings in immediate and dramatic

reduction of dysfluencies in DS (e.gs., Andrews et al., 1983; Freeman & Armson, 1998; Saltuklaroglu,Kalinowski, Robbins, Crawcour, & Bowers, 2009). Recently, Balasubramanian et al. (2010) investi-gated the choral reading effect in two subjects with ANS. However, in contrast to the findings from DS,their subjects failed to show any noticeable improvements in speech fluency under this task.

Despite the dramatic reduction of dysfluencies under choral/unison speech in DS, the mechanismbehind this effect remains elusive. Yet, it has been proposed that the underlying mechanism in choralreading is similar to the rhythm effect while singing. That is, like rhythm in singing, voice of theaccompanist provides external timing cues during speech production (Alm, 2004; Büchel & Sommer,2004). An alternate explanation for the fluency enhancement under choral reading in PWS has beenoffered by Kalinowski and Saltuklaroglu (2003). These authors proposed that choral speech effect isa form of direct imitation, a primitive and innate human capacity that is possibly mediated by themirror neurons systems (see Kalinowski & Saltuklaroglu, 2003, for details).

1.1.4. Altered auditory feedbackThe auditory feedback refers to the cortical processing mechanism for speech production that

occurs when the produced message is compared and verified with the intended message while thespeaker’s auditory system perceives his/her own speech output. The term ‘altered auditory feedback’(AAF), therefore, refers to alterations to recurrent auditory information (Howell, 2004).

Three forms of AAF have traditionally been used to modify the dysfluencies in PWS viz. a) maskedauditory feedback (MAF); b) delayed auditory feedback (DAF); and c) frequency-shifted auditory feed-back (FAF). In MAF, the speech of the speaker is simultaneously and constantlymasked by an additionalsignal (e.g. white noise). In DAF, speakers hear their own speechwith a short time delay (50–250ms). InFAF, the frequency range of the speakers’ speech is shifted either up or down leading to changes in theperceived pitch (for a recent review on AAF, see Antipova, Purdy, Blakeley, & Williams, 2008).

In the early years, the occasional observations of reduced dysfluencies in the presence of loud noiseset the stage for MAF research in stuttering (Bloodstein, 1995). Ever since these early observations,diverse effects of the binaural presentation of continuous masking noise on dysfluencies in PWS havebeen reported. For instance numerous studies (e.gs., Andrews et al., 1983; Bloodstein, 1995; Lincoln,Packman, Onslow, & Jones, 2010; Martin, Johnson, Siegel, & Haroldson, 1985; Van Riper, 1982) repor-ted of significant reduction in dysfluencies under MAF, and some have even reported of completeeradication of dysfluencies (e.g., Cherry, Sayers, & Marland, 1955). However, interestingly, a few studies(e.gs., Block, Ingham, & Bench, 1996; Lincoln et al., 2010) reported of an increment, rather thana reduction in dysfluencies under MAF in a portion of their participants.

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Yet another interesting observation from some of the early studies is the gradual reduction ofdysfluencies with the gradual increment in masking noise level (e.g., Maraist & Hutton, 1957).Specifically, these authors reported that the number of dysfluencies in their DS subjects (N ¼ 15)reduced from 26 to six as the masking noise was raised from zero to 90 dB (sensation level). It may,however, be noticed that even at 90 dBSL, the dysfluencies did not completely vanish in their subjects.Supportive evidences for the reduction of dysfluencies with increment inmasking noise level were alsoreported by the later researchers (e.g., Martin, Siegel, Johnson, & Haroldson, 1984).

In a recent study, Lincoln et al. (2010) compared the effects of various alterations in auditoryfeedback in the speech of PWS with that of the non-altered (normal) auditory feedback condition. Atthe group level (N ¼ 11), these authors observed significant reduction in dysfluencies under MAF(condition – 7; see below). Additionally, four participants of their group showed maximum reductionin dysfluencies under MAF compared to various combinations of DAF and FAF. Contrastively, anotherfour participants of their study group showed an increment in dysfluencies under MAF. From theirstudy, Lincoln et al. (2010) concluded that although at the group level, the dysfluencies showedreduction under various auditory feedback conditions (MAF included), at the individual level, thedysfluencies varied across the tasks, as is evident from their observations of four participants showingmaximum reduction, whereas another four showing an increment in dysfluencies under MAF.

Together these observations suggest that the mechanism of variation in dysfluencies under MAFremain highly elusive and its effect could vary across the PWS. Barring the counter-observations (i.e.,increased dysfluencies; Block et al., 1996; Lincoln et al., 2010), the reduction of dysfluencies under MAFhas been attributed to the complete blockage of auditory feedback (e.gs., Andrews, Howie, Dozsa, &Guitar, 1982; Van Riper, 1982). The gradual reduction in dysfluencies with the increment in maskingnoise level (e.gs., Maraist & Hutton, 1957; Martin et al., 1984) supports this hypothesis. Yet theobservations that subjects under MAF could still hear their speech (e.g., Adams &Moore, 1972) supportthe hypothesis that MAF reduces the quality of the auditory feedback, rather than completely elimi-nating it (e.g., Starkweather, 1987).

The hypothesis that the dysfluency reduction results from the alteration in the quality of theauditory feedback rather than its elimination paved the way to DAF and FAF research in stuttering. Forinstance, Antipova et al. (2008) systematically varied the FAF and DAF in a group of eight people withDS and found that the maximum reduction in stuttering (35%) was seen at 75 ms which rose to 44%with addition of 1½ octave downward shift in frequency. Recently, Lincoln et al. (2010) investigated thecombined effects of DAF and FAF in a group of 11 people with DS. Specifically, these authors studied thevariation in stuttering under eight different conditions (i.e., 1 – control [Normal Auditory Feedback –

NAF]; 2 – Min FAF þ Min DAF; 3 – Max FAF þ Max DAF; 4 – Max FAF þ Min DAF; 5 – Min FAF þ MaxDAF; 6 – Max FAF þ Max DAF [reading]; 7 – MAF [white noise]; and 8 – control reading [NAF]) andreported of maximum reduction in dysfluencies under conditions 6 (Max FAF þ Max DAF [reading])and 5 (Min FAF þ Max DAF) at the group level. However, the results of dysfluency analysis at theindividual level revealed marked variations in the responsiveness of the participants to differentfeedback conditions. These findings were, in accordance with previous investigations (e.gs., Armson &Kiefte, 2008; Armson & Stuart, 1998; Ingham, Moglia, Frank, Ingham, & Cordes, 1997) that reportedindividual variability in dysfluency reduction under AAF. It is apparent from the survey of literaturethat the systematic investigations of ANS under MAF are surprisingly lacking.

Unlike MAF, there have been certain literature evidences on FAF and DAF in ANS. For instance,Balasubramanian and Max (2008) reported the case of a 59-year-old patient with post-stroke aphasiawhose speech was characterized by stutter-like part-word repetitions and hesitations. These authorsrequired their subject to read a 200-word text under four conditions: 1) reading with non-alteredfeedback; 2) reading with 50 ms DAF; 3) reading with increased (1/2 octave) FAF; and 4) reading withdecreased (1/2 octave) FAF. Analysis of the speech fluency revealed that reading under these fourconditions failed to enhance fluency. Interestingly, the authors observed slightly higher dysfluenciesunder the AAF conditions compared to the control condition.

In yet another recent study, Balasubramanian et al. (2010) reported an increment, rather thanreduction in stuttering under AAF in two subjects with ANS. In the first subject, no apparent variationin stuttering under DAF compared to normal auditory feedback was observed. However, in the samepatient, shifting the auditory feedback either half octave up or down resulted in an increment, rather

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than reduction in stuttering. The second subject failed to show dysfluency reduction under both DAFand FAF conditions. The authors attributed these differential performances under fluency-enhancingconditions by their subjects to the differences in underlying neurological bases of fluency disorder andalso to the available neural resources that could be recruited to benefit from these fluency-enhancingconditions.

Van Borsel et al. (2010) investigated the effects of DAF in a 49-year-old man with ANS. In thespontaneous speech task, the speech rate varied with the changes in feedback delay. That is, theirsubject showed an increased rate of speechwhen the feedbackwas delayed by 70ms, whereas, the ratereduced with the delay of 110 ms. Further, there were qualitative differences in the nature of dys-fluencies across the feedback conditions. In the non-altered feedback (normal) condition, the majortypes of dysfluencies in spontaneous speech were filled pauses and syllable and word repetitions. Inthe reading task, under the normal feedback condition, syllable and word repetitions along withbroken words dominated the dysfluency types. However, under DAF conditions, both reading andspontaneous speech tasks showed increased prolongations as well as word and phrase repetitions withthe reduction of filled pauses. From these observations, Van Borsel et al. (2010) argued that DAF mayhave different effects in individuals with ANS and DS, possibly revealing the heterogeneity in theunderlying pathology between these two types of fluency disorders.

In the next section, we proceed to the neural substrates of (dys)fluent speech in stuttering, primarilyderived from the functional neuroimaging studies. Herewe review the evidences from the DS literaturesince such studies have seldom been reported in ANS population.

1.2. Functional neuroimaging investigations of stuttering

The recent advances in functional neuroimaging are, undeniably a promise to the stutteringresearch. For the last 10–15 years, evidences of altered functional integrity of the CNS structures in PWShave been accumulating from the Positron Emission Tomography (PET), Magnetoencephalography(MEG), and functional Magnetic Resonance Imaging (fMRI) paradigms employed in stuttering research(Krishnan, Nair, & Tiwari, 2010). However, such investigations are primarily performed in DS and,therefore, the applicability of the information derived from such studies in ANS, is debatable (VanBorsel et al., 2010). In the following section, we briefly review the pertinent functional neuro-imaging studies in (developmental) stuttering.

Employing the positron emission tomography (PET) technique, Fox et al. (1996) provided evidencefor increased right hemisphere activation in a group of PWS. In the subsequent year, Braun et al. (1997)replicated this result and further opined that the activity in the left hemisphere was increased duringthe production of stuttered speech, whereas, the activation of the right hemisphere correlatedwith thefluent speech. Together these studies, therefore, proposed that the primary dysfunction is located inthe left hemisphere and that the hyperactivation of the right hemisphere indicated a compensatoryprocess, rather than the cause of stuttering (e.g., Brown, Ingham, Ingham, Laird, & Fox, 2005).Corroborative evidences for the right hemisphere hyperactivity associated with fluent speechproduction have been reported by other investigators (e.g., Neumann et al., 2003). A recent study byWatkins, Smith, Davis, and Howell (2008) extended the neural bases of dysfluent speech from thecortical to subcortical structures (basal ganglia) in stuttering. These authors stated that stuttering isassociated with the disruption of the cortico-subcortical neural systems supporting the selection,initiation, and execution of motor sequences necessary for fluent speech production.

In a very recent study that investigated the interactions among the neural structures in the basalganglia-thalamocortical circuit of the left hemisphere, Lu, Peng, et al. (2010) found both anatomical andphysiological differences between people with and without stuttering. The major physiologicaldifferences in PWS group were: the weaker negative connectivity from the posterior middle temporalgyrus to the putamen; stronger positive connectivity from the putamen to the thalamus and fromthalamus to the posterior middle temporal gyrus as well as to the anterior supplementary motor area;and finally from the anterior superior temporal gyrus to the anterior supplementary motor area of theleft hemisphere. Anatomically, PWS were characterized by increased gray matter volume concentra-tion in the left putamen and reduced gray matter volume concentration in the left medial frontal gyrusand anterior superior temporal gyrus as well as reduced white matter volume concentration in the

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posterior superior temporal gyrus inside the basal ganglia-thalamocortical circuit. Thus, Lu, Peng, et al.(2010) provided evidences for the connectivity differences not only between the ganglio-thalamic andfronto-temporal cortices, but also for the circuits within the subcortical (i.e., putamen to thalamus) andcortical (i.e., posterior middle temporal gyrus to anterior superior temporal gyrus and then to the pre-supplementary motor area [pre-SMA]) structures. The altered functional connectivity among thesestructures was further substantiated by the structural equation modeling (SEM) and voxel-basedmorphometry (VBM) employed in their study.

It is, therefore, apparent from these neuroimaging investigations that PWS differed from normalsubjects anatomically and physiologically (i.e., connectivity) not only at the cortical but also at thesubcortical level. In the light of such functional neuroimaging-derived information, we briefly reviewthe recent explanatory hypotheses of dysfluent speech in DS.

1.3. Neural bases of dysfluent speech in DS

In an extensive review, Alm (2004) delineated the association between stuttering and basal ganglia(BG) structures. Specifically, Alm proposed that the basal ganglia play a crucial role in internal timingcues for the initiation of the subsequent motor segments in speech. That is, the supplementary motorcortex (SMC), which is important for the internal timing cues, receives inputs from the basal ganglia,whereas, the premotor cortex, a vital structure for external timing cues, receives inputs from thecerebellum. The improvement in motor performance with external cues in subjects with Parkinson’sdisease has been projected as an evidence for the spared cerebellar–premotor cortex connections andimpaired basal ganglia-SMC circuits. Corroborative evidences have also been reported from a recentneuroimaging study (Lu, Chen, et al., 2010) indicating that the atypical planning and execution ofmotormovements during speech production in PWS is due to the dysfunctional basal ganglia-inferior frontalgyrus/premotor area and cerebellum-PMA circuits. Unlike the previous studies with evidences fromsubjects with Parkinson’s disease, the participants in Lu, Chen, et al.’s (2010) study included a group of12 subjects with the age of stuttering onset ranging from three to 12 years. Thus, these authors couldextend the role of impaired basal ganglia from Parkinson’s disease to DS.

To account for the variations in speech fluency under altered auditory feedback, Alm (2004)reviewed and compiled two explanatory hypotheses viz. a) de-automatization and b) reduction offeedback gain. The de-automatization account posits that the somatosensory and auditory feedbacksinput to the putamen (Yeterian & Pandya, 1998), which in turn, facilitates the BG to execute automatedor programmed movement sequences on habituated environmental context (Wise, Murray, & Gerfen,1996). Altering the auditory feedback, therefore, is expected to lead to de-automatization. Thereduction of feedback gain hypothesis posits that the signal overflow in the sensory-motor loop isreduced when the auditory feedback is masked, thereby leading to the reduction in stuttering. Alter-natively, Max et al. (2004) suggested that altering (masking) the feedback effectively shuts down thefeedback circuit, which, in turn, leads to the inconsistent perception of the speaker’s own speech.Following Paus, Marrett, Worsley, and Evans (1996), Max et al. (2004) further reasoned that theexternal auditory stimulation may activate the auditory cortex that increases the activation of theinternal models used to monitor efference copies (i.e. information from ongoing motor neuron activitysent to other regions of the nervous system: Imamizu, 2010) of themotor commands. That is, activationof the auditory cortex by the external auditory stimuli is thought to improve the efficiency of feedbackmonitoring by improving the feedback controller’s predictions of the auditory consequences of plan-ned movements, leading to improvements in speech fluency.

Collectively, it is apparent from the brief review above that ANS is less likely to be a homogenousgroup as its clinical features vary across the subjects as well as fluency-enhancing conditions (e.gs.,Balasubramanian et al., 2010; Jokel et al., 2007; Tani & Sakai, 2010b; Theys et al., 2008; Van Borsel et al.,2010) possibly due to the variability in the underlying mechanisms. Further, the neuroimaging studieson DS have provided insights about the various neuroanatomical substrates, especially the role of basalganglia in fluent speech production. A review of literature has surprisingly shown no attempts toexplain the clinical manifestations of ANS in the light of these recent neuroimaging evidences from DS.In this context, the present study attempts to fit the clinical profile of a patient with ANS into theexplanatory hypotheses derived from DS.

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2. Materials and methods

2.1. History, neurological, and neuroradiological examinations

A 56-year-old, right-handed lady was admitted to our hospital with the complaints of sudden-onset, right-sided weakness with unclear and stutter speech. At the time of admission, she wasconscious, alert, and oriented to place, person, and time. The history revealed an earlier episode ofstroke (2 months ago) which was associated with loss of consciousness, vomiting, and residual righthemiparesis with unclear and stutter speech. The weakness on the right side subsided in less than oneweek post-onset. However, her speech difficulties did not subside on par with themotor weakness. Shewas treated in a local hospital subsequent to this episode. The second and current episode was asso-ciatedwith vomiting and vertigo for a fewminutes. She did not experience loss of consciousness duringthis episode. The weakness on the right side recurred with the aggravation of the residual speechdifficulty. At the onset of the current (second) episode she was able to walk with support from twopersons. However, while reporting to our hospital, on the third post-onset day, she was able to walkwith minimal support from one person. Her pulse rate was 80/min and blood pressure was 140/90 mmHg on admission. The cranial nerve examination was unremarkable except the CN-VII uppermotor neuron palsy on the right side. The motor power on the left side was normal, whereas, the sameon the right side was Grade 4 with slightly elevated reflexes. She did not reveal any sensory deficits onthe right side. On the second day of admission, even before medication was started, she reportedfurther improvement in her motor power in the right limbs. However, the speech difficulty reportedlydid not subside. A magnetic resonance imaging study on the second day post-admission revealed aninfarct in the left putamen. Administration of the Edinburgh Handedness Inventory (Oldfield, 1971)revealed that the subject was a strong right hander (þ100).

2.2. Assessment of communication skills

The subject was referred to the Neuro-Communication Disorders Unit (NCDU) of the Department ofSpeech and Hearing for a detailed evaluation of her communication skills. The formal assessment of herlanguage functions with the Malayalam version (Philip, 1992) of Western Aphasia Battery (Kertesz,1982) revealed intact linguistic skills. Administration of the Apraxia Battery for Adults (Dabul, 1979)did not reveal any apraxic errors. However, she exhibited hyperkinetic dysarthria (Frenchay DysarthriaAssessment; Enderby, 1983). Her speech was characterized by distorted vowels, irregular articulatorybreakdowns, excess and alternating loudness, strained and strangled voice with intermittent stop-pages, variable rate, prolonged intervals, inappropriate silences, excess and equal stress, impreciseconsonants, and overall reduced speech intelligibility. These features were indicative of the involve-ment of articulatory–phonatory–prosodic aspects of the speech production system, suggestive ofhyperkinetic dysarthria. Further, the involuntary movements of the face, neck, and occasional whole-body movements substantiated the diagnosis of hyperkinetic dysarthria. The maximum phonationtime was reduced to 10 s with intermittent voice breaks indicative of the phonatory instability. Thequality of phonation was strained and low-pitched.

To assess the speech fluency, 3-min conversational speech and reading samples were collected. Tocheck the adaptation effect, shewas required to read the passage consecutively for five times. However,she read it only four times, owing to her inability to read further. We also collected the reading sampleunder masking noise (presented binaurally at 90 dB SPL), 5 dB below the uncomfortable level (MaicoMA 52 Audiometer) and 1-min singing sample under normal auditory feedback. The subject did notcomply with any further testing procedure owing to her discomfort while speaking. All task perfor-mances were video-recorded (Sony DCR-SR300) and later transcribed by an experienced speech-language pathologist in the area of neurogenic communication disorders (first author).

Additionally, to rule out the psychogenic origin of dysfluencies in speech, psychiatric consultationwas recommended. However, shewas unwilling to undergo for the same. In this context, we performedseparate informal interviews with the subject and her caretaker (daughter) to rule out the possiblepsychogenic origin of speech dysfluencies. Both did not report of any significant family issues in thepast. The subject had a healthy relationship with her spouse and children. All her children were well-

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settled in their life. Conversely, the onset of the disorder was during a pleasant family occasion(marriage of a relative).

Based on the above finding, our subject was diagnosed to have acquired neurogenic stuttering withhyperkinetic dysarthria. Subsequently she was enrolled for speech therapy (45 min, daily) for a periodof one week. From our observations during the assessment as well as from the subject’s own opinion,the dysfluent speech was more disabling than the dysarthric errors. Therefore, we decided to focus onreducing the dysfluencies in speech. Yet another reason for not prioritizing the hyperkinetic dysarthriafor speech therapy was the previous proposal of relatively meager effect of behavioral (speech) therapyin people with hyperkinetic dysarthria (Duffy, 2005).

2.3. Speech therapy

We employed the pacing technique to modify her dysfluent speech and the subject respondedeffectively to this technique. She attended seven 45-min therapy sessions with a frequency of onesession/day during her hospital stay. At the end of the seventh session, a 3-min conversation andpassage reading revealed fluent speech with occasional involuntary movements of the corner of thelips that did not apparently interfere with the speech. The subject and her daughter expressed satis-faction with the improvements in the former’s speech.

3. Results

The results of dysfluency analyses showed marked dysfluencies during conversation, reading withnormal auditory feedback, and repeated reading of the passage and marked dysfluency reductionunder masked auditory feedback and while singing (see Tables 1 and 2, for details).

4. Discussion

The subject in the present study exhibited two episodes of sudden-onset right hemiparesis withunclear and stutter speech. Within the first week of the initial episode, the motor deficit hadcompletely subsided with insignificant recovery from speech disturbances. The second episode ofstroke, two months later, resulted in the relapse of the recovered right limb motor functions andfurther worsening of the residual speech skills. The assessment of communication skills revealed thepresence of ANS with hyperkinetic dysarthria. Extended assessment of the speech fluency undercertain fluency-enhancing conditions revealed certain riveting features. In the following section, wediscuss these features and attempt to fit our observations into the recent explanatory models derivedfrom functional neuroimaging studies in DS.

However, before we continue, a differentiation between hyperkinetic dysarthria and ANS in oursubject deems necessary. We ascertain that the observed dysfluencies were due to the presence of ANSrather than due to hyperkinetic dysarthria as these showed variations under various fluency-enhancing conditions. The speech disruptions associated with hyperkinetic dysarthria, on the other

Table 1Rate of speech as well as the types and distribution of dysfluencies during conversation and reading tasks.

Conversation Reading

Rate of speech (M ¼ 117; SD ¼ 16 wpm)a 78 71Dysfluency types and %Syllable repetitions 11.11 14.06Part-word repetitions 6.48 12.5Blocks 5.56 6.25Prolongations 4.63 12.5Phoneme repetitions 2.78 3.13Phrase repetitions 2.78 3.13Hesitations 1.85 4.68Total 35.19 56.25

a Combined (conversation þ reading) values (Savithri & Jayaram, 2008).

Table 2Dysfluency types and percentage across the three fluency-enhancing conditions.

Dysfluency types and % MAF Repeated readings Singing

Trial 1 Trial 2 Trial 3 Trial 4

Syllable repetition 4.68 13 11 13 12 2Part-word repetitions – 12 12 14 13 –

Blocks – 6 9 8 8 –

Prolongations – 12 10 11 10 –

Phoneme repetition 1.56 3 2 5 2 –

Phrase repetition – 3 2 2 3 –

Hesitations – 4 3 3 3 –

Total % 6.24 53 49 56 51 2

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hand, do not show such variations under fluency-enhancing conditions. Further, following thesuccessful recovery from dysfluencies, our subject exhibited occasional involuntary movements of theoro-facial complex, confirming the presence of residual hyperkinetic dysarthria.

The subject exhibited marked stuttering both in spontaneous speech and reading tasks (see Table1). Yet, it may be noticed that she exhibited maximum dysfluencies while reading compared tospontaneous speech. Such variations in dysfluencies in different tasks have been reported in theprevious studies as well. For instance, three of five people with ANS in Tani and Sakai’s (2010b) cohortalso exhibited maximum dysfluencies while reading compared to other tasks such as explanation ofcomic strips and repetition. The reason for such differential effect of tasks on dysfluencies remainselusive. Although the present study is unable to delineate this differential effect, we consider certainpossibilities. For instance, compared to the spontaneous speech task, reading invites a multitude ofadditional sensory and cognitive operations such as identifying the graphemes, deriving theirphonology and finally constructing the visual word form of the read word, which in turn, is followed bythe conceptual activations (in the case of knownwords) (Price &Mechelli, 2005). In this context, it maybe possible that these additional operations may impose greater demands on the cognitive systemduring the reading task leading to the increased dysfluencies in PWS.

The subject in the present study exhibited apparent reduction in dysfluencies under MAF andsinging conditions. Interestingly she failed to show the adaptation effect (see Table 2). Further, it mayalso be noted that the dysfluencies in speech were completely eliminated with the pacing techniqueduring speech therapy. A few studies in the recent past have shown that subjects with ANS do not showenhanced fluency under AAF conditions (e.gs., Balasubramanian & Max, 2008; Balasubramanian et al.,2010). Further, it has been suggested that in ANS, the responses to various fluency-enhancing condi-tions differ from subject to subject. In this context, the marked reduction in dysfluency under MAFcondition in our subject may be attributed to two reasons. First, we employed MAF condition ratherthan DAF or FAF, like in the previous studies (Balasubramanian & Max, 2008; Balasubramanian et al.,2010). Second, in Balasubramanian et al.’s (2010) study, the failure of the two subjects to show anidentical pattern of responses under the AAF conditions (i.e., DAF & FAF) was attributed to thedifferences in underlying neurological bases of fluency and also to the available neural resources thatcould be recruited to benefit from these fluency-enhancing conditions. If these were the cases, thereduction in dysfluency under MAF in our subject may also be attributed to the variability in theunderlying neurological bases of fluency (discussed later). Additional testing of speech fluency underFAF and DAF may have been more informative in the present study. However, owing to the patient’snon-compliance with the further testing, we could not investigate it.

The lack of adaptation effect in our subject was in accordance with the observations fromBalasubramanin et al.’s (2010) study. Their subjects showed only minimal improvements in fluencywith repeated readings of the passage. The subject in the present study did not show any apparentvariation in speech fluency (see Table 2). The adaptation effect in DS has been attributed to the practiceeffect, which facilitates the internal timing cues in the basal ganglia (Alm, 2004). In this context, theabsent adaptation effect in our subject may, therefore, be attributed to the structural damage to thebasal ganglia, rendering the practice effect ineffective. The seemingly disparate observations of Taniand Sakai (2010b) with the present study necessitate the need for further research into the specific

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role of basal ganglia in adaptation effect. This is specifically relevant in the context of high inter-subjectvariability (e.g., Tani & Sakai, 2010b) in adaptation effect among people with ANS. That is, instead ofdrawing a correlation between basal ganglia damage and the absence/presence of adaptation effect, itmay be constructive to investigate the specific effect of distinct basal ganglia structures such as caudatenucleus, putamen, and globus pallidus on adaptation effect, either through an anatomo-clinicalcorrelation approach or through functional neuroimaging techniques.

Summing up the observations from the current study, it is apparent that, with the exception ofadaptation effect, our subject revealed enhanced fluency underMAF, singing and pacing tasks. All thesetasks are known to enhance fluency in subjects with DS (e.g., Andrews et al., 1982). Does such partiallyoverlapping clinical profile with the DS indicate similarity in the underlying neural substrates betweenthese two types of dysfluency disorders? In the following section, we address this issue in the light ofrecent functional neuroimaging evidences from DS.

The recent explanatory models of DS, largely derived from the functional neuroimaging research,have unambiguously recognized the role of cortico-subcortical network in fluent speech production (Luet al., 2009). Specifically, Alm (2004) proposed two types of timing cues (internal & external) that engagebasal ganglia-pre-supplementary cortex and cerebellar–premotor cortex, respectively. These twonetworks are proposed to play distinct roles in the fluent speech production (Alm, 2004). Extrapolatingthese proposals into the observations from our subject, the marked stuttering instances during spon-taneous speech and reading tasks may be considered as evidence for the impaired internal timing cuesassociatedwith the damaged basal ganglia system. That is, in the absence of additional (external timing)cues, the subjectmayhave relied on the impairedbasal ganglia-pre-supplementarymotorareanetwork,leading to dysfluent speech. In contrast to this, the enhancement of speech fluency while singing andspeaking with pacing technique may be attributed to the employment of two additional mechanisms.First,while singing, the internal representationof the rhythmmayhaveprovided the internal timing cuesnecessary for the initiation of each syllable (i.e., the rhythm effect; Alm, 2004), facilitating the fluentspeech production. Corroborative evidence for this proposal has been reported by Jeffries et al. (2003),who demonstrated that speech engaged mainly left hemisphere areas, whereas, singing involvedextensiveactivationof the righthemisphere. Further, these authorsnoticed that the speech task stronglyactivated the left putamen, whereas, singing task activated neither left nor right putamen. In the light ofthese observations, it may be argued that, in our subject with basal ganglia lesion, the enhanced fluencywhile singing may have recruited right hemispheric structures to facilitate the rhythm-related cues.Distinctly, the fluency enhancement with pacing technique may be attributed to the rhythm effect,through the external timing cues (i.e., cerebellar- pre-SMAnetwork) as this task, unlike singing, doesnotinitiate the syllables (Alm, 2004). In brief, the enhanced speech fluency during singing and pacing, andmarked dysfluency during conversation and reading supported the recent explanatory hypotheses onthe role of cortico-subcortical network in fluent speech production.

Under MAF condition, our subject showed an apparent reduction (but not elimination) of speechdysfluencies. Several explanatory hypotheses may account for this observation (see Introduction). Forinstance, the reduction in stuttering under MAF in the present study may be attributed to the de-automatized execution of motor sequences resulting from the elimination of auditory feedbacksubsequent to the lesion in the basal ganglia. However, we could not determine if our subject’s stutterspeech had already become automatic in nature, so that when the auditory feedback was masked, thesystemwas de-automatized, leading to fluent speech production. The reduction of sensory feedback gain(Alm, 2004), on the other hand, seemed to provide a viable explanation, especially in the light of ourobservations that the stuttering instances were not completely eliminated byMAF. That is, reduction ofsensory feedback by the presentation of themasking noisemay have reduced the signal overflow in thesensory-motor loop, leading to reduction in stuttering. It may also be possible that both these mech-anisms (i.e. de-automatization and reduction of sensory feedback gain) may have together producedthe reduction in stuttering in our subject (Alm, 2004).

The reduction in stuttering in our subject under MAF is also in agreement with Max et al.’s (2004)proposal that masking noise may have shut down the feedback circuit, leading to inconsistentperception of the subject’s own (dysfluent) speech, which in turn, lead to the reduction in stuttering.Further, this is also in support of the early proposals of Starkweather (1987) that the masking noisealters the quality of auditory feedback. Recent studies have provided supplementary evidences that

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overreliance on auditory feedback could lead to sound/syllable repetitions (Civier, Tasko, & Guenther,2010; Tourville, Ghosh, Reilly, & Guenther, 2008).

However, Max et al.’s (2004) hypothesis that stuttering reduces by improving the efficiency of thefeedbackmonitoring mechanismwith the activation of the auditory cortex through the presentation ofan external auditory stimulus seemed unlikely in our subject since the auditory feedback was masked,rather than delayed or frequency-shifted, in the present study. Therefore, our observations suggest thatthe reduction in stuttering under MAF may be attributed to: a) the reduction of sensory feedback gain(that may have either reduced the signal overflow in the sensory-motor loop or shut down the auditoryperception of inconsistent motor sequences [dysfluent speech] produced by our subject); b) de-automatization of motor sequences; or c) a combination of a and b.

Before we proceed to the limitations of the current study, a note on the disparate findings onperformance under various fluency-enhancing conditions by the subjects with stuttering is worthconsidering. It is apparent from the review of previous investigations that people with ANS exhibitextreme variability under various fluency-enhancing conditions (e.gs., Balasubramanian et al., 2010;Jokel et al., 2007; Tani & Sakai, 2010b; Theys et al., 2008; Van Borsel et al., 2010). For instance, inTani and Sakai’s (2010b) study, all subjects with ANS exhibited positive adaptation effect, although itwas variable across them. However, the subject in the present study failed to exhibit the adaptationeffect despite of the marked reduction in dysfluencies under tasks like MAF, singing, and pacing. Insimilar lines, Lincoln et al.’s (2010) observation that four participants with DS exhibited maximumfluency underMAF, whereas, another four exhibited increased dysfluency under same condition showsthat people with DS also show such task-related variability. Together these observations from both ANSand DS as well as the past evidences (e.gs., Armson & Kiefte, 2008; Armson & Stuart, 1998;Balasubramanian et al., 2010; Ingham et al., 1997; Jokel et al., 2007; Tani & Sakai, 2010b; Theys et al.,2008; Van Borsel et al., 2010) show that the individual variability is the hallmark of dysfluenciesunder fluency-enhancing conditions. In Balasubramanian et al.’s (2010) view, the variability may beattributed to the differences in underlying neurological bases of fluency and also to the available neuralresources that could be recruited to benefit from these fluency-enhancing conditions. In this context,we propose that investigating the neural correlates of such variability may be more productive thansearching for the distinct dysfluency profile specific to each type of stuttering (i.e., ANS & DS). Perhaps,the application of functional neuroimaging techniques in ANS, especially when such investigations aresurprisingly lacking in this disorder, may provide potential insights in this regard.

Finally, we acknowledge the limitations of the present study. First, the possibility of psychogenicnature of stuttering could not be categorically ruled out in our subject as she was reluctant to undergopsychiatric evaluation. However, the available history superseded the possibility of psychogenicstuttering. For instance, the subject had a pleasant and healthy relationship with her spouse andchildren. Neither the subject nor her daughter (caretaker) reported of any significant family issues thatcould lead to the current manifestation. All her childrenwerewell-settled in their life. Additionally, thetime of onset of her speech disturbances was during a pleasant family event. Finally, the neurologicalexamination and neuroimaging investigation revealed the presence of structural lesion in the nervoussystem and the presence of hyperkinetic dysarthria supported the definite involvement of the basalganglia circuit in our subject. Second, an in-depth investigation of dysfluencies in our subject undervarious other fluency-enhancing conditions may have made our results readily comparable withprevious similar studies. However, owing to the subject’s non-compliance with additional testing, wecould not perform those tasks. Lastly, an inherent limitation of this study was that the currentobservations are from a single subject. Yet, considering the fact that systematic and extended clinicalinvestigations on ANS are largely lacking in the literature, we argue that vital and novel observationsand attempts to fit them into the existing theoretical models, such as in the present study, are of greatimportance to the scientific community. Such observations may eventually pave the way to large groupstudies in a systematic manner, which in turn, is the need of the hour in the realm of ANS.

5. Conclusion and future directions

The present study showed certain routine and extended clinical observations from a subject withANS. Despite the marked dysfluencies during spontaneous speech and reading, our subject exhibited

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apparent reduction in dysfluencies under MAF, singing, and pacing tasks. However she failed to exhibitthe adaptation effect. Further, we have shown that the recent explanatory hypotheses of DS couldlargely explain the clinical observations from our subject with ANS. The current study, therefore,highlighted certain novel observations in ANS as well as the applicability of hypotheses derived fromDS in ANS. However, in the context of apparent variability in dysfluencies under various fluency-enhancing conditions, especially at the individual level, future studies may consider large samples.Finally, we advocate comparative functional neuroimaging investigations in subjects with ANS and DSwhich may test the generality of the DS-derived hypotheses into ANS. Such investigations may alsoshed light on the neural correlates of variability in dysfluencies under various fluency-enhancingconditions in people with ANS and DS.

Source of funding

None.

Conflicts of interest

None.

Acknowledgments

The authors thank the subject and her daughter for their co-operation and participation in thepresent study. They also thank Dr. B. Rajashekar (Dean, MCOAHS, Manipal) and Dr. S.N. Rao (HOD, Dept.of Neurology, Kasturba Hospital, Manipal) for their valuable help.

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