brain imaging and stuttering: some reflections on current and future developments

Journal of Fluency Disorders28 (2003) 411–420

Commentary

Brain imaging and stuttering: some reflectionson current and future developments

Roger J. Ingham∗

Department of Speech and Hearing Sciences, University of California,Santa Barbara, CA 93106, USA

Received 15 August 2003; accepted 19 August 2003

Keywords:Stuttering; Brain imaging; Treatment

This special edition is a tribute to the Editor’s foresight in recognizing that thisis an opportune time to review the status of the now burgeoning brain imagingstudies on stuttering. His idea was to try to bring together some of the currentcontributors to that research by inviting papers from laboratories that are cur-rently conducting brain imaging investigations of developmental stuttering. Eachcontributor was given a very wide mandate as to what to present. The invitationsimply requested a manuscript that described current research in their particularlaboratory and, if possible, share with theJournal of Fluency Disordersreadersthe direction of their research. There was no expectation that the authors wouldpresent completed research, but preliminary findings were certainly encouraged.It’s quite obvious, therefore, that the contributors more than met the terms of thatrequest. The result is a series of papers that constitute an illuminating overviewof the different imaging techniques and strategies that are now being used to in-vestigate stuttering — and the implications of the findings for theory and therapy.They contain a number of themes. Included are accounts of studies designed tounderstand the neural processes associated with the language of persons who stut-ter, theoretic accounts of the current array of findings and their relevance to otherdisorders, studies designed to isolate regional activations and deactivations asso-ciated with the fluency-inducing procedures and those associated with treatment.

∗ Tel.: +1-805-893-2776; fax:+1-805-893-4431.E-mail address:[email protected] (R.J. Ingham).

0094-730X/$ – see front matter © 2003 Elsevier Inc. All rights reserved.doi:10.1016/j.jfludis.2003.08.003

412 R.J. Ingham / Journal of Fluency Disorders 28 (2003) 411–420

It was not possible to obtain contributions from researchers using techniques otherthan functional magnetic resonance imaging (fMRI) or H2

15O positron emissiontomography (PET). Consequently readers should be aware that other researchersare conducting studies on stuttering using magnetoencephalography (MEG) (e.g.,Salmelin, Schnitzler, Schmitz, & Freund, 2000) or MRI to elucidate the neu-roanatomic characteristics of stuttering speakers (e.g.,Foundas, Bollich, Corey,Hurley, & Heilman, 2001).

In many ways the studies described in this special edition have only just begun torealize the enormous promise of brain imaging for the investigation of stuttering.For this writer that promise first appeared with the publication of the groundbreaking PET investigations byPetersen, Fox, Posner, and Raichle (1988)andPetersen, Fox, Posner, Mintun, and Raichle (1989). These studies were the first toshow the different neural regions throughout the brain that are activated by readingsingle words, saying those words and generating new words (verb generation). Inmany respects the findings dramatically verified and enriched earlier theoreticmodels of the neural system that operates during speech production. They alsocame at a time when it was becoming increasingly obvious that stuttering mustinvolve abnormal neural processing of speech. Suggestions that this was the casewere alluded to in earlier EEG studies (e.g.,Boberg, Yeudall, Schopflocher, &Bo-Lassen, 1983; Moore, 1984), but it also became apparent that the source(s)of some of the phenomena that characterize stuttering (e.g., chorus reading) wasnot going to be understood by focusing solely on peripheral processes (Ingham,1998). The Petersen et al. studies were a revelation; they suggested that PET couldhelp to isolate the particular neural regions that are functionally associated withstuttering, especially because it could be used in conjunction with fluency-inducingstrategies. Later techniques and methods — especially performance correlationanalysis (Silbersweig et al., 1995) — added to the promise by suggesting that itmight be possible to identify the specific regions that change in conjunction withthe frequency of stuttering. Has that goal been achieved? Only partially it seems.

It is clear from the preceding articles that the unusual right hemisphere activa-tions that occur during stuttered speech do recede with treatment or fluency induc-ing strategies, and there is general agreement that there is a lack of activation in thetemporal lobe region. However, there is also marked variability across the findings.In fact, it seems clear that the variety of methodologies used to investigate the neuralprocesses associated with speech may strongly influence the clarity of the findings.

For a while the variability or inconsistency in findings from many imagingstudies on speech and language raised concerns about their validity (Poeppel,1996; but seeDémonet, Fiez, Paulesu, Petersen, & Zatorre, 1996). That certainlyprompted some vigorous efforts to rectify the inconsistencies (Hickock, 2001) —although recent meta-analyses now suggest that they are much less problematic(Fox et al., 2001; Turkeltaub, Eden, Jones, & Zeffiro, 2002). Nevertheless, there aresome unresolved methodological problems thatGrabowski and Damasio (2000)contend continue to impact straightforward comparisons among the findings ofdifferent imaging studies. They identified at least four such problems:

R.J. Ingham / Journal of Fluency Disorders 28 (2003) 411–420 413

1. The problem of paradigm design: The uncertain stability of a cognitive stateacross the experimental and control conditions within subtraction designs.This is whatBoring (1950)described as the “pure insertion” problem withinsubtraction designs;

2. The obstacles to fine-grained anatomical interpretation of results: The vari-ability between individual anatomy and its transformation into “Talairachspace” (Talairach & Tournoux, 1988) anatomy, including variability acrossstudies in mapping Talairach coordinates to regions (seeBrett, Johnsrude,& Owen, 2002);

3. The problem of implicit assumptions about the signal in which one is in-terested: Differences among the various smoothing filters that are usedto improve the signal-to-noise ratio and which may affect the spatial andtemporal shape of responses (seeWhite et al., 2001);

4. The problem of negative results: By using conservative statistical thresholdsto avoid false positive activations, imaging may demonstrate systems thatparticipate in task performance, but they do not necessarily fully identifythe sufficient systems.

An overview of the papers in this special edition suggests that these unresolvedproblems might explain much of the variability across their findings. For instance,the subtraction design is a feature of most of the studies. However,Stager, Jeffries,and Braun (2003)have also used performance correlation techniques, which offsetmuch of the pure insertion problem (see alsoFox et al., 2000; Ingham et al., inpress). With respect to the second problem, some imaging studies use StatisticalParametric Mapping (SPM 99;Wellcome Department of Cognitive Neurology,1999) to identify activated regions, but others use rather different techniques (e.g.,Lancaster et al., 2000). Problems 3 and 4 are especially interesting: There is literallyno consistency across these studies with respect to the choice of image smoothingfilters and the statistical thresholds that have been selected certainly vary widely.Of course, this list might be augmented because of the use of different imagingtechnologies. For instance, the three labs reporting on treatment studies (De Nil,Kroll, Lafaille, & Houle, 2003; Ingham, Ingham, Finn, & Fox, 2003; Neumannet al., 2003) have used very different imaging techniques and tasks. The projects re-ported byNeumann et al. (2003)have used event-related fMRI, while those byDeNil et al. (2003)and the San Antonio group (Ingham et al., 2003) have usedH2

15O PET. In addition, the speaking tasks have ranged from reading singlewords, reading short sentences, through to continuous oral reading and mono-logues — with and without the presence of stuttering events. Consequently somedifferences among the findings should not be too surprising — and especiallyin light of the history of imaging studies of language function. After review-ing those studiesGrabowski and Damasio (2000, p. 445)reached the followingsobering conclusion: “When two functional imaging studies attempt to isolate aspecific language-processing component using different tasks, the results usuallydiffer.”


Despite a variety of methodologies and techniques, there is an emerging con-sensus among the contributors’ studies about the brain areas that are implicatedin stuttering — or in the neural areas that stuttering speakers employ duringspeech-related activities. That consensus points to excessive neural activation inthe right hemisphere involving the right operculum and especially the regionsrelated to speech motor behavior. In addition there is compelling evidence thatthis abnormal neural activity is associated with an underactivated auditory sys-tem; possibly contributing to whatLudlow and Loucks (2003)described as “asystem dysfunction that interferes with rapid and dynamic speech processing forproduction.” The presence of excessive right hemisphere or bilateral activationappears to be prompted by lexical retrieval tasks that do not involve overt speechproduction (seeBlomgren, Nagarajan, Lee, Li, & Alvord, 2003), which, in turn,may relate to the effect of lexical factors on stuttering (Prins, Main, & Wampler,1997). The relationship between level of activation in the motor-auditory regionsand the production of overt stuttered speech is still unclear. However, the use ofdifferent fluency-inducing strategies, such as chorus reading, metronome-trainedspeech, singing, or prolonged speech, appears to substantially normalize the re-gional activations in the motor-auditory region.Stager et al. (2003)suggest thatthis could be due to “a common fluency-evoking mechanism (that) might relate tomore effective coupling of auditory and motor systems — that is, more efficientself-monitoring, allowing motor areas to more effectively modify speech.” Thatobservation is certainly consistent with findings emerging from studies conductedby this writer and colleagues. It is also generally consistent with the findings ofstudies that have evaluated the neural activity associated with the outcome of pro-longed speech-related treatments. Complicating matters, however, are the markeddifferences in the activation patterns obtained from two of these studies at the pointof treatment outcome evaluation.De Nil et al. (2003)reported that the “lateralizedbias for some areas shifted as subjects first completed intensive therapy and sub-sequently the maintenance phase.” By contrast,Neumann et al. (2003)found thatthe overactivations immediately after therapy “were more widespread and morebilaterally distributed than before. . . (but at) . . . follow-up the majority of theoveractivations had shifted back to the right hemisphere, but remained still morewidespread than before therapy.” Neumann et al.’s finding may also be partiallyconsistent with suggestions that some abnormal activations continue to be evidentamong individuals who appear to have fully recovered from stuttering (Inghamet al., 2003). Of course the differences between De Nil et al. and Neumann et al.’sfindings might simply reduce to the levels of efficacy of two different treatments.

One of the recurring issues surrounding brain imaging research on differentdisorders is the extent to which the findings can contribute to treatment — oneof the important themes in this collection of papers. In the case of stuttering, forinstance, the present findings give no indication as to how the regional activations(and deactivations) that support stuttered speech might be changed. It is certainlyinteresting to know that treatment might help to normalize the neurophysiologicalprocesses associated with speech production in normally fluent speakers, but is


that of much value if there is continuing uncertainty about the durability of thebenefits of the treatments under investigation? For that reason there seems to besome merit in the careful investigation of persons who have fully recovered fromstuttering — especially those who have fully recovered by self-managed strategies.It seems reasonable to speculate that these individuals might demonstrate the extentof neural system change that is possible through behavior change and perhaps thespecific changes that are necessary to support normal fluency.

It is obvious that brain imaging researchers have focused much of their attentionon treatment — but only treatment for adults. That focus, of course, is largely dueto restrictions that apply to the use of invasive imaging techniques with children.But it also applies to noninvasive techniques, which, in the case of fMRI, requirea young child to be confined for lengthy periods within an MR scanning tunnel.Until this problem is fully solved then questions concerning the age when unusualor abnormal activations appear cannot be addressed.

The initial attempts to identify the neural processes associated with adult ther-apy have also brought forth other issues. For instance, the only stuttering treatmentsthat have been investigated using brain imaging are those utilizing some variantof prolonged speech (Ingham, 1984). But even those variants involve much morethan prolonged speech training.De Nil et al. (2003)used subjects treated by thePrecision Fluency Shaping (PFS) program (Webster, 1974), which trains speakersto use syllable prolongation, soft voice onset, and reduced articulatory gestures.Neumann and colleagues have conducted their research in conjunction with a ther-apy program known as the Kassel Stuttering Therapy or KST (Euler & Wolff vonGudenberg, 2000). KST is a modified version of the PFS utilizing computer-aidedtraining and a structured 1- to 2-year maintenance program.Ingham et al. (2003)used the Modified Phonation Interval (MPI) program (Ingham et al., 2001) whichuses computer-aided training to reduce the frequency of short phonation intervals inconjunction with self-managed performance-contingent transfer and maintenanceschedules. There is also an obvious difference between the speech tasks used duringscanning and the speech tasks required to evaluate therapy effects. The speakingtasks used during scanning conditions may have external or ecological validity, butthat has yet to be demonstrated. Nonetheless, even if this was demonstrated to bethe case, then imaging data derived from therapy might ultimately constitute littlemore than a surrogate outcome measure necessarily supplemented by measures ofspeech performance.

An alternative way in which imaging research on stuttering might advance isthrough the investigation of strategies for directly modifying the neural system.Exploratory studies on the use of transcranial magnetic stimulation (TMS) (seeHallett, 2000, for a review) may offer that promise, but in ways that are not yet fullyunderstood. Earlier TMS studies by our group were directed towards stimulatingneural sites that PET imaging had shown might be implicated in stuttering (seeIngham, Fox, Ingham, Collins, & Pridgen, 2000). An initial attempt at the modi-fication of supplementary motor area activity (based onFox et al., 1996) did notproduce beneficial effects. However, a concurrent investigation (Fox et al., 1997)


that used TMS to explore neural connectivity in healthy subjects did highlightthe technique’s immense diagnostic potential. Indeed, this has since become anestablished strategy for identifying neural connectivity (seeSieber & Rothwell,2003). TMS can also used to determine if the perturbation of an aberrant circuit hasshort-term clinical effects. An interesting application of this strategy was recentlyreported byTopper, Foltys, Meister, Sparing, and Boroojerdi (2003)with respectto phantom limb pain. The use of this technique to identify aberrant neural circuitsin adult stuttering speakers and then assess the modifiability of those circuits isnow being explored by our group. That research is also benefiting from the de-velopment of vastly improved methods for aiming the TMS stimulator at specificregions. The perturbation strategy might also serve to fully explore the circuitrywithin models of the speech production system, such as that proposed byJürgens(2002 — also see Ingham et al., 2003). That same strategy might also be useful forexploring the full implications ofSalmelin et al.’s (2000)intriguing MEG finding;that is, that the order of neural regions are activated in speech production typicallyfollows a Wernicke’s area→ Broca’s area→ M1-mouth path in normal speakers,but among stuttering speakers the path (for producing nonstuttered words) wasfound to be Wernicke’s area→ M1-mouth→ Broca’s area. This study clearlyhighlights the importance of neural pathways. It is worth pointing out, however,that MEG shares with TMS an important limitation — currently both techniquesare unsuitable for investigating subcortical regions of the brain. The perturbationstrategy will therefore require other techniques to elucidate the system that ulti-mately produces stuttered speech.

As mentioned earlier, neuroanatomic investigations of stuttering are not repre-sented among the special edition papers. Recent neuroanatomic investigations havereported that stuttering speakers (adults) display structural abnormalities (Foundaset al., 2001) or lesions (Sommer, Koch, Paulus, Weiller, & Büchel, 2002). Butthe findings portray a complex picture. Sommer et al. reported focal abnormali-ties in the white matter of the left frontal operculum in stuttering speakers usingdiffusion-weighted MRI. They interpreted their findings as evidence of atrophyof myelinated fibers connecting speech-related regions of the superior tempo-ral lobe with those of the frontal lobe. Although the abnormality reported bySommer et al. is in the same general region (left inferior frontal lobe) as that re-ported by Foundas et al., the findings from both studies are difficult to reconcile.Foundas et al. reported larger structures and more gyri; Sommer et al. reportedatrophy. Further, although T1-weighted MRI images were acquired in Sommeret al.’s subjects (the image type used by Foundas et al.), no abnormalities of T1images were reported, suggesting a failure to confirm Foundas et al.’s findings.On the other hand, both studies found abnormalities in approximately the samebrain region, a region strongly implicated in speech production. One possible ex-planation for these somewhat conflicting reports is that no single type of brainanomaly underlies all cases of developmental stuttering. Lesion type may varybased on genetics (or other factors), with lesion location being the more criticalvariable.


Much recent imaging research has been aimed at finding powerful methodsfor influencing neural plasticity — both functional and anatomical plasticity —and this may have immense implications for stuttering research (Taub, Uswatte, &Elbert, 2002). Kochunov et al. (2003)recently observed that these may be inherentproperties of the human brain. “Functional plasticity,” as they note (p. 961), “refersto the dynamic changes in functional organization of a system that are driven byan adaptation to a novel stimulation or acquisition of a new motor skill.” Forthe most part the focus of attention in this area has been on understanding thefactors that may influence change in the somatosensory, auditory, visual and motorsystems — such changes do appear to have occurred among recovered stutterers(seeIngham et al., 2003). However, as Kochunov et al. also point out, there isnow convincing evidence that cortical anatomical plasticity may also occur as aresult of a variety of experiences, usually of extensive duration.Amunts et al.(1997), for instance, showed that the normal left–right asymmetry in the size ofthe precentral gyrus was substantially more symmetrical in professional pianists,especially in the hand area and Kochunov et al. identified intriguing anatomicaldifferences in Asian and Western speakers. Thus it is interesting to consider thepossibility that a lifetime of chronic stuttering may impact anatomic structure andthereby impact the possibilities of behavior change and the neural systems that arefunctionally associated with stuttering. Nevertheless, recent studies showing thesuccess of Constraint-induced Therapy (Liepert et al., 2000; Taub & Morris, 2001)with stroke patients — many of whom suffered their stroke at least a decade earlier— suggest that the limits of neural plasticity in adults are far from established(Taub et al., 2002). In short, the age-dependent limits on recovery may be morespeculative than real — and may depend on finding similar techniques for inducingneural plasticity in adult stuttering speakers.

Predicting the future is always hazardous and often of little value, but it can helpto etch out goals and expectations. And, in the case of imaging research, these canbe reasonably derived from a history that has been largely driven by technologicaldevelopment and discovery. Cerebral blood flow has undoubtedly provided neuralresearchers with a powerful tool for investigating neural processes. And the searchfor methods to measure and track that flow will continue to improve the use ofthat tool. But neural systems can also be monitored and measured by other means,including electroencephalography and neural transmitters. Of far more interest,however, has been the development of tools for modifying neural system activity.Drug research continues to provide the dominant source of interest for producing atherapeutic interaction between the neural system and behavior change — but thebenefits from drug research for stuttering are still uncertain (seeLudlow & Loucks,2003). Meanwhile, research on methods for changing behavior without drug inter-vention will undoubtedly benefit from further refinements to MRI, PET and TMS.And there is also little doubt that radically different approaches will emerge fromwithin the exciting advances in nanotechnology, stem cell research and genetics.

There are numerous exciting possibilities for assisting research on the theoryand treatment of stuttering. At the forefront, however, must be the development of


a neural systems model of stuttering, based on carefully derived empirical studiesof speech production tasks that characterize stuttering and its variability — ratherthan one based on preconceived theoretic constructs. This is the route proposed inPeter Fox’s (2003)provocative paper and it seems to offer the most promise fora dramatic breakthrough in this area of research. Another is the need to conductimaging studies on children who are at risk for stuttering and those who recoveror do not recover from stuttering within the first few years after onset. This iscertainly possible with creative studies using fMRI that might also help to identifythe formation of the aberrant system that supports chronic stuttering. The need forinvestigations of stuttering treatment has already been discussed. But there is alsoa need to investigate the interaction between neural systems (including structure)and treatment responsiveness. Studies in these areas are urgently needed if imagingresearch on stuttering is going to fully realize its early promise.

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brain imaging and stuttering: some reflections on current and future developments

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