Stuttering is a disorder of speech fluency that presents itself between the ages of 2 and 4 years. In the preschool population, the incidence is approximately 5% and the prevalence in the general population is 1%.

An early and influential theory of the brain basis of stuttering holds that its underlying cause is anomalous hemispheric lateralization of the speech control centers. Specifically, Orton (1927) contends that, in contrast to fluent speakers, people who stutter (PWS) have bilateral representations for speech processes. In their schema, rather than a single dominant (left) hemisphere producing speech, in the person who stutters both hemispheres issue commands which, when not perfectly synchronized, cause the blocking and repetition of speech segments that characterize stuttering. Despite the substantial face validity of this hypothesis, extensive behavioral testing of motor behavior in stutterers provides scant support. Work in the 80s and 90s by Webster (1985, 1986) converged on the position that “people who stutter have normal left hemisphere lateralization of the neural mechanisms for the control of speech and other forms of sequential movement” (Webster, 1997), findings that concur with sodium amytal tests of cerebral dominance for speech and language in PWS. As described by Andrews et al. (1972) and Luessenhop et al. (1973), PWS respond to right- and left-sided carotid artery injections of sodium amytal in the same way as fluent speakers. Such direct evidence supports the contention that PWS have a normal pattern of hemispheric specialization for speech.

Despite such findings, the theory that abnormal speech control lateralization drives stuttering still has currency in the general discourse around stuttering (e.g., Kushner, 2012). The perpetuation of this idea is supported in part by the findings from brain imaging evidence that has emerged in the past 20 years (for review, see Brown et al., 2005). A common finding in a number of these studies is a shift of speech-related brain activity to the right hemisphere in adults who stutter. In their seminal PET study, Fox et al. (1996) report increased activation in the right hemisphere in a language task in developmental stutterers. This finding was subsequently replicated by Braun et al. (1997), who were able to differentiate between patterns of stuttered and fluent speech in the stutterers that they tested. Importantly, their results challenge the idea that abnormal laterality caused stuttering. By demonstrating that the left hemisphere was more active during the production of stuttered speech and the right more active with fluent speech, the authors were able to conclude that the primary dysfunction in stuttering is located in the left hemisphere. They further suggested that hyperactivation of the right hemisphere is therefore not the cause of stuttering, but rather a reflection of neuroplastic adaptation.

Such compensatory plasticity has a well-established precedent in the lesion literature where transference of function between hemispheres has been observed in (e.g., Weiller et al., 1995). Following on from the early PET studies of stuttering, a subsequent fMRI investigation by Preibisch et al. (2003) showed that overactivity in the right frontal operculum in PWS was negatively correlated with stuttering. Furthermore, this overactivation was evident even when speech tasks were not required. Taken together, these observations support the idea that overactivation in the right hemisphere seen with functional neuroimaging in PWS reflects a compensatory mechanism rather than being a manifestation of abnormal cerebral dominance for speech control (e.g., Braun et al., 1997; Preibisch et al., 2003; Chang et al., 2008; Lu et al., 2010).

There is a missing piece in this puzzle that might help adjudicate between causal and reactive origins for hemispheric activation anomalies in stuttering. Given that stuttering emerges most commonly in the preschool years, observation of normal hemispheric laterality of brain activity during speech production would support the thesis that increases in the right hemispheric activation in adults who stutter are the result of compensatory mechanisms developed over a lifetime of stuttering. At present, there is no functional brain imaging evidence from children near the age of onset of stuttering. The present study was designed to provide such evidence.

The current results are the first functional brain imaging data of overt speech production in preschool-aged CWS. This is an important contribution to a literature based on results from older children and adults, whose brain functions have had many years to develop compensatory strategies.

There is a long history of attributing the cause of stuttering to atypical laterality of speech/language function. The roots of this theory can be traced back to publications in the early twentieth century by Orton (1927) and Travis (1931), hence the lateralization theory of stuttering often being referred to as the Orton–Travis theory. They posited that a failure in development of normal cerebral dominance would lead to cascade of events: competition between the hemispheres, an incoordination of outputs and interruption of fluent speech. Even though the early attempts to test this theory experimentally were inconclusive (Bryngelson, 1935, 1939; Heltman, 1940) and a number of negative findings followed, e.g., Dorman and Porter (1975), interest in the theory has persisted, most likely because of its parsimonious appeal and the persistence of anecdotal evidence suggesting that forced changes in handedness for writing – a common educational practice in the early twentieth century (Kushner, 2012) – gave rise to stuttering or that left handedness conveys a higher risk for stuttering. Indeed, it is still common to find examples such claims as “Most stammering children are left-handed” (du Plessix Gray, 2012) or “In fact, just as human speech – stuttering in particular – is related to cerebral laterality (most stutterers are left-handed)…” (Shell, 2006), in the popular press, despite significant evidence to the contrary (Records et al., 1977; Webster and Poulos, 1987; Ardila et al., 1994; Salihovic and Sinanovic, 2000). While the burgeoning neuroimaging literature on stuttering has conferred some support for the idea that anomalous laterality is the cause of stuttering, such imaging data cannot provide a causal link. Indeed, it has long been contended that right hemispheric overactivations represent reactions to, or compensations for stuttering, rather than being causative agents. For this reason, anatomical or functional demonstrations of normal laterality in young stutterers are powerful evidence against a laterality origin for stuttering and would support a reactive origin for the changes in both functional and structural laterality changes seen in adult stutterers. Our data strongly support the contention that the laterality anomalies of older stutterers reflect compensatory shifting of function rather than an underlying causal dysfunction. This conclusion is supported by a recent neuroanatomical study that reported no differences in right–left asymmetries between 9- and 12-year-old stuttering boys and a matched cohort of controls (Chang et al., 2008).

An important caveat to this conclusion comes from the fact that a significant proportion of those children who begin to stutter will spontaneously recover [up to 80% by some estimations (Yairi and Ambrose, 1992, 1999; Yairi et al., 1993; Kalinowski et al., 2002)]. With this in mind, it is possible that our child participants may be quite different neurologically from children whose stuttering persists into adulthood. That is, while the sample we tested were all current stutterers at the time of our investigation, it must be expected that most of them would not continue to be stutterers into adulthood and therefore a large proportion of our sample consists of stutterers who will recover precisely because they do not have the underlying abnormal laterality that leads to persistent developmental stuttering. This possibility is encapsulated well in the work of Shell (2006) who states, “Particularized lateralization among human children develops ontogenetically at around the time they are learning to speak. Some researchers think this fact may explain why so many children (3–4%) “stumble” in speech and then “outgrow” the problem when lateralization is fully developed. Those children who do not fully lateralize are, according to this view, the children who are the “real” stutterers (about 1%).” Arguing against this possibility, the study by Chang et al. (2008) showed that the brains of recovered stutterers were more like those of current stutterers than control subjects, an observation that suggests that the occurrence of recovery likely reflects initial severity rather than reflecting the existence of a neurologically distinct subgroup. For this reason, we believe our data are still likely to reflect the true status of laterality in the early stages of stuttering, at least in regard to speech production.

The possibility remains though that anomalous laterality of other speech or language-related brain functions might exist in the early stages of stuttering. Indeed, a recent study using near infrared spectroscopy suggests that this may be the case in regard to some aspects of auditory language processing (Sato et al., 2011). Future studies looking to characterize brain activation anomalies in young CWS should include longitudinal following of the subjects so that retrospective analysis of those subjects whose stuttering does not resolve might be carried out. Given a large enough initial cohort, this approach would allow researchers to control for possible heterogeneities within the cohort.

While the interpretation of child MEG data in source space must be considered in light of the inherent uncertainties that govern solutions to the inverse problem, the concordance between the results of the whole-brain analysis presented herein and previous MEG studies of speech in adult subjects suggests that these findings are robust. In the time after early visual processing, and consistent with articulatory planning for speech (Levelt et al., 1998), a strongly left-lateralized brain network was activated. This network consisted of inferior frontal, parietal, and temporal nodes largely consistent with previous MEG studies that have examined speech or speech planning (e.g., Carota et al., 2010). Notably, our results show a distinctly left-lateralized inferior frontal activation, and premotor activity in areas consistent with the SMA activity seen in previous studies (Salmelin et al., 1994, 2000). Furthermore, like the study of Salmelin et al. (2000), the activity we saw in the SMA was right lateralized. We also observed significant parietal lobe activations in our study which, while not consistent with the fMRI literature on overt speech (Indefrey and Levelt, 2004), is consistent with similar MEG studies, which have consistently found activation in both inferior and superior parietal lobes (Salmelin et al., 1994; Levelt et al., 1998; Hulten et al., 2009) including Brodmann area 7 (Carota et al., 2010), which was the most active parietal locus in our findings. Carota et al. (2010) suggest that activation in Brodmann area 7 during speech planning is indicative of the parietal cortex’s key role in monitoring motor intention in language.

Our conclusions regarding the lack of laterality differences must be considered within the scope of the limited part of the speech planning process that we have examined. It is important to emphasize that the time window beyond 600 ms was not taken into inversion analysis and, given that the average vocal reaction time was longer than 1000 ms, there remains a significant epoch in which laterality differences might manifest. It is, however, important to note that articulatory mouth movement begins significantly earlier than the onset of overt speech – similar studies to the current one suggest this difference is in the order of 300 ms in adult subjects (Salmelin et al., 2000) hence the speech planning time is not as long as the reaction time as measured by voice key as in the current study. Future development of devices, which allow real-time monitoring of articulatory movements within the MEG environment (e.g., Lau, 2013) should allow for articulatory artifacts to be controlled much more precisely and remove a number of the limitations surrounding the time frame in which brain processing of speech production might be measured.

A number of previous neuroimaging studies using hemodynamic techniques (PET, fMRI) have shown there to be differences between stutterers and non-stutterers in the activation strength of various cortical and subcortical sources (e.g., Fox et al., 1996, 2000; Braun et al., 1997; De Nil et al., 2000, 2008; Ingham et al., 2000; Neumann et al., 2003; Preibisch et al., 2003; Giraud et al., 2008; Watkins et al., 2008; Chang et al., 2009; Kell et al., 2009; Sakai et al., 2009; Loucks et al., 2011); (for review, see De Nil and Kroll, 2001; Ingham, 2001; Fox, 2003; Brown et al., 2005). However, our study did not find any difference between source activation strength between CWS and TD. This difference may reflect a difference between neuromagnetic approaches to source imaging compared to hemodynamic imaging. Indeed, most previous MEG studies of stuttering have not attempted to analyze differences in source activations, rather utilizing the inherent temporal advantage of MEG to illustrate differences in auditory evoked activations (Salmelin et al., 1998; Beal et al., 2010; Kikuchi et al., 2011b) and temporal dynamics (Salmelin et al., 2000; Biermann-Ruben et al., 2005) or location of discrete dipole sources (Salmelin et al., 2000). Only a single previous study has demonstrated the ability of MEG to characterize cortical activation patterns in stuttering using a distributed sources model, and that was in a single adult subject (Sowman et al., 2012). Our primary aim was to use the other advantages of MEG (passivity, lack of noise, and reduced need for enclosure of the participant) to investigate laterality in children. A previous MEG study using a similar approach has shown that left dominance of parietotemporal coherence in theta band activity is specifically correlated with higher performance of language-related tasks in preschool children (Kikuchi et al., 2011a). The current study also demonstrates the utility and possible sensitivity of MEG-based measures for characterizing laterality in developmental language disorders.

In conclusion, we have demonstrated that in the very early stages of stuttering development, the preparation for speech is not characterized by anomalous lateralization of brain activations. This evidence gives weight to the hypothesis that the right hemispheric biases in chronic stuttering are due to neuroplastic adaptations rather than being an underlying primary source of dysfunction.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.