tDCS – a novel means for the treatment of stuttering

This post is about the article “Transcranial direct current stimulation over left inferior frontal cortex improves speech fluency in adults who stutter” by Jennifer Chesters, Riika Möttönen, and Kate E. Watkins, recently published online in the journal Brain – see here (free full text).

The authors applied transcranial direct current stimulation (tDCS) to the left inferior frontal cortex during speech production in combination with choral reading and metronome-timed speech. They found a significantly greater and more lasting effect of the fluency training combined with tDCS as compared with the same fluency training combined with sham stimulation.

The authors propose “that tDCS over the left inferior frontal cortex during the fluent mode of speaking facilitated plasticity of the frontal speech network and prolonged its normalized functioning, resulting in lasting improvements in fluency.” I completely agree with this explanation, and it is amazing that this could be shown after a fluency training of only five days with sessions of twenty minutes a day.

However, six weeks after intervention, the reduction of stuttering in conversation had decreased significantly also in the tDCS group. It is therefore, important to find out how the fluency training can be improved – it may not be sufficient to only extend the duration of training and tDCS. We should therefore ask what exactly happens during chorus reading or metronome-timed speech. What is the effect depending on, and how can a similar effect be achieved in everyday talking?

The role of the left inferior frontal gyrus

Chorus reading as well as metronome-timed speech were shown to transiently normalize the activation in the left inferior frontal gyrus (IFG, Broca’s area), associated with a reduction or elimination of stuttering. But not only the left IFG is under-activated during stuttered speech, the left auditory cortex (Wernicke’s area) is under-activated too, and also this is normalized by chorus reading and metronome-timed speech (see Table 1 on my website for an overview). There seems to be a relationship between left IFG activation and auditory activation during speech.

Fibers of the superior longitudinal fasciculus terminate in the IFG (see, e.g., Makris etal, 2005), and we can assume that the IFG is involved in the processing of auditory feedback information provided via that fiber tract. This processing, and by that, auditory-motor integration may be impaired when the left IFG is under-activated during stuttered speech. However, the immediate efficacy of chorus reading and metronome timing on speech fluency suggests that the left-hemispheric speech network is quite able to work well if certain requirements are met – which is obviously the case during chorus reading and metronome-timed speech. But what requirements are that?

Chorus reading and metronome-timed speech

Some researchers believe that the speaker gets clues for syllable starts, which helps stutterers because they have difficulty generating their own speech rhythm. But that is not plausible for at least two reasons. First, chorus reading and metronome-timed speech cannot function in the way that the speaker each time reacts to a signal from outside. If you, at each time, wait until you hear the beat of the metronome, or until you hear the co-speakers starting a syllable, and only then say the syllable yourself, then you will never be synchronous but always too late because of the reaction time. Instead, you are required to capture the given beat or pace so that you can predict and anticipate it. Then you must adjust your own pace to the given pace and continuously monitor whether you are still in sync with the metronome or the co-speakers. That is, you must attentively listen to both, the given pace and your own speech, in order to correct your pace if necessary.

Therefore, chorus reading and metronome-timed speech do not only make the speaker listen to the externally given beat or pace, but also listen to his/her own speech. In this way, these conditions improve the processing of auditory feedback (the processing of verbal input is attention-depending – see below) and by that, auditory-motor integration is improved, which results in fluent speech.

A second argument against the hypothesis people who stutter benefit from external cues for syllable starts is that they are quite able to generate their own rhythm, for example, in singing as well as in speaking accompanied by rhythmic arm/hand movements. This is confirmed by an experiment conducted by Howell and El-Yaniv (1987): Adults who stutter were reading a short story (1) normally, (2) while listening to the clicks of a metronome and (3) while listening to clicks occurring at the beginning of every syllable, triggered by the intensity of the speaker’s voice (i.e., it was the participant’s self-generated rhythm). The third condition reduced stuttering nearly as effectively as the second one: The mean number of disfluencies on average in the story was 20.25 in the normal condition, 0.6 with metronome, and 2.5 with click at syllable onset.

The background: attention allocation in motor behavior

Complex automatized sequential motor behavior, e.g., in manual working, sports, dancing, playing music, driving a car, etc., and also speaking requires the ongoing integration of sensory input, among them sensory feedback, in several modalities (visual, acoustic, tactile, kinesthetic) and with that the appropriate allocation of perceptual- and processing capacities for the respective behavior or task. I simply call this the allocation of attention, even if the person often is not aware of it, as it is an integral component of the behavior and was learned and automatized together with that motor ability.

Errors in automatized sequential behavior occur if the appropriate allocation of attention is disturbed or was not correctly learned. For example, attention may be distracted from sensory input, or overly focused on one component of the sensory input, e.g., on one sensory modality. In speaking, the first happens when the speaker is overly focused on the thoughts or emotions that shall be expressed, or on the fear of disfluency; the second happens when the speaker is too much focused on the feedback of articulatory movements (e.g. in the attempt to avoid stuttering) to the detriment of the auditory component and/or the proprioception of breathing.

I propose that developmental stuttering is caused by a misallocation of attention, that is, of perceptual- and processing capacity during speech. The misallocation may be due to several factors (see my last post in this blog), but chorus reading and metronome-timed speech seem to be tasks which compel the speaker to reallocate his/her attention, namely: to listen during speech – not only to the co-speaker or to the metronome, but also to his/her own speech.

Consequence for treatment
In chorus reading and in metronome-timed speech, the speaker is compelled to reallocate attention, but might mostly not become aware of this fact, especially not of the fact that he or she must listen not only to the co-speaker or the metronome, but also to his/her own speech. Thus the reallocation of attention is not maintained in everyday talking. One goal of therapy should therefore be to make clients aware of the necessity to reallocate attention during speech, and to practice listening to one’s own words in everyday situations.

Lateralization of the processing of verbal acoustic input is depending on attention (it is left-lateralized only during active listening; Poeppel et al.,1996; Rämä et al., 2012; Sabri et al., 2008), and particularly on attention to the lexical aspect of speech (attention to the prosodic or sound aspect draws processing to the right hemisphere; Hugdahl etal., 2003; Vingerhoets, Berckmoes, and Stroobant, 2003). What is true for the processing of external verbal input might also be true for the processing of auditory feedback. It is therefore important to listen not only to one’s own voice, but to one’s own words.

In this way, it should be possible to maintain a normal activation of the left-hemispheric speech network, and transcranial direct current stimulation seems to be a good means that can support this by promoting a change in brain structure.

Persistence versus recovery of stuttering

In this post, I want to sketch some ideas about the development of stuttering. Today stuttering is often called a neurodevelopmental disorder, which might be correct, however, the brain is plastic, especially in young children, and its development interacts with learning and with the development of behavioral habits and routines.

A part of behavior often overlooked is the allocation of attention, that is, of perceptual and processing capacity during motor tasks, including speaking. In my theory of stuttering, I assume that just this mostly unconscious aspect of behavioral control is the crucial causal factor. The figure below shows the hypothesized development from stuttering onset to recovery (persistent stuttering is not included in this figure). The colors mean: blue = developmental steps, red = causal factors, yellow = triggers or secondary negative factors, green = positive factors.

Transient developmental stuttering

I think the cause of childhood stuttering, in most cases, is an imbalance in the development of sensorimotor integration, namely to the favor of action and to the detriment of perception and feedback processing. This becomes problematic in the change to connected speech and sentence production which requires a stronger involvement of auditory feedback and the feedback of breathing in speech control – the brain must perceive and keep in memory which constituents of a sentence have already been produced in order to correctly complete the sentence, and breathing times must be included in the speech sequence.

Of course children are not aware of changing behavior when they start forming sentences. Empirical findings suggesting such an imbalance in the attention system are

• a high number of dopamine D2 receptors at age 2.5 to 3 (Alm 2004, Fig. 2; see also Rothmond et al. 2012, Fig. 3), associated with a tendency towards generally high motor activity;
• lower fractional anisotropy (FA) in the left arcuate fasciculus, probably indicating delayed fiber maturation (see Fig. 1, Cluster 1 and 2 in Chow and Chang, in press – interestingly, these clusters of lower FA were much larger in the recovered group than in the persistent group). The structural deficits might be the manifestation (rather the result than the cause) of poor involvement of sensory feedback in motor control.
• atypical network connectivity in children who stutter (persistent as well as recovered) compared to controls. See Fig. 5 in Chang et al (2018), especially the reduced connectivity between Dorsal Attention Network and Default Mode Network and the hyperconnectivity between Ventral Attention Network and Default Mode Network, indicating an imbalance in the control of attention. Interestingly, there was even found a reduced connectivity in the visual network in stuttering children (Fig. 4), suggesting a general deficit in the involvement of sensory input in the control of behavior.  

The idea that the onset of stuttering in most cases is related to the beginning of connected speech and sentence forming is not new. Bloodstein (2006) pointed to the facts that “early stuttering occurs only on the first word of a syntactic structure; stuttering does not appear to be influenced by word-related factors; early stuttering seldom occurs on one-word utterances; the earliest age at which stuttering is reported is 18 months, with the beginning of grammatical development; the age at which most onset of stuttering is reported, 2-5 years, coincides with the period during which children acquire syntax; considerable spontaneous recovery takes place at the time most children have mastered syntax; incipient stuttering is influenced by the length and grammatical complexity of utterances...”
 

A further suggestion to an imbalance in development as a causal factor comes from the observation that not a few children with early-onset stuttering show syntactic abilities and length of utterances well above the norm for their age (Watkins, Yairi, and Ambrose, 1999). Alm(2004) writes about that: “The group with early onset stuttering, who entered the study at age 2-3, showed syntactic abilities and length of utterances well above what was expected for their age. In fact, in some aspects the language abilities in this group were on a level with the norms for 2 years older children. This was true both for children who recovered and for children who persisted to stutter.” Too much attention (capacity) may be taken by sentence planning, and too little attention may remain for perception and feedback processing in these children.

Late-onset stuttering and the so called ‘psychogenic stuttering’ was included in the above figure because I think that cause and pathomechanism are the same as in developmental sttutering, but affected individuals seem to have no strong predisposition for stuttering, especially not for persistent stuttering. But in a person whose attention system is vulnerable, strongly negative emotions, distress, fear, or the aftermath of a trauma may result in a misallocation of attention during speech and by that in stuttering. Complete recovery is often reached in such cases by a supporting environment and/or by therapy, including psychotherapy that helps coping with traumatic experiences (see Table 1 in Chang et al.,2010).

Spontaneous recovery in general may be caused by a kind of unconscious learning effect: Children eventually learn to adapt their attentional allocation, that is, the allocation of their perceptual and processing capacity to the new demands of connected speech and sentence production. Such a learning effect manifests in brain structure: See, e.g., the upward trajectories of FA for the recovered group in Fig. 1 (Cluster 3 and 5), and Fig. 2 (Cluster 6) in Chow andChang (in press). I interpret those changes in brain structure as consequences of learning since several studies have shown that even a few weeks of practice (e.g., in reading, juggling) result in changes of gray or white matter structure (see Section 4.1 on my website).

When I assume that most stuttering children eventually learn to adapt their attentional allocation to the demands of connected speech. then this doesn’t mean they all learn to behave completely in the same way as children who have never stuttered do. The results depicted in Fig. 6 in Chang et al. (2008) suggest that the left brain hemisphere played a minor and the right one a greater role in speaking in the children who had recovered from stuttering, compared to the normal fluent controls. The cause could be that speech control in the recovered children, on average, was not as automatic (i.e., more volitional) as in normal fluent children. 

I don’t like to speak of compensation in the brain here, because there is no little manager sitting in the brain who notices a dysfunction and bids another part of the brain to sub. It is rather the child who becomes aware of a problem and tries to cope with it, and this behavior, over time, results in a structural change in the brain.

Persistent developmental stuttering

 

If my above ideas about transient stuttering are true, then the question arises: Why does a minority of the children affected by stuttering not learn to adapt their attention to the demands of connected speech? Is there an additional causal factor impairing the allocation of attention in these children? In fact, there seems to exist such a factor: a subtle deficit in central auditory processing. Many empirical findings point in this direction (see Section 3.3.1 for an overview). Unfortunately, we have data about auditory processing in persistent stuttering only, but not in individuals who recovered. 

 Unfortunately, there are few data comparing auditory processing in those who persisted in stuttering and in those who recovered. The only study I know is by Howell, Davis, and Williams (2006) who compared children of both groups in a backward-masking task the performance or which is assumed to reflect the operation of central auditory processing, especially of temporal structure. They found an appropriately 10 decibel higher mean backward-masking threshold in the persistent group. The difference was statistically significant, but there was a high variability in the persistent group, thus the authors conclude that an auditory deficit may be sufficient, but not necessary, for the disorder to persist.
 

Further, Usler and Weber-Fox (2015) and Mohan and Weber (2015) found differences between children with persistent stuttering and those who recovered in the processing of auditorily presented verbal stimuli. Furthermore, Chow and Chang (in press) found a structural deficit (lower FA) in fibers of the splenium, i.e., the posterior part of the corpus callosum in children who eventually persisted in stuttering, but not in those who eventually recovered (see Fig. 1, Cluster 4 in the study). The affected fibers probably connect bilateral temporal regions (Kuvazeva, 2013), and lower FA may be related to a less effective labor division between hemispheres in auditory processing.

The difference in FA in the mentioned cluster is great already with the youngest children, and there is no much overlap between the persistent group, on one hand, and the recovered and control group, on the other hand. Therefore, the deficit can hardly be a consequence of stuttering. Interestingly, Chow, Liu, Bernstein Ratner, and Braun found a strong relation between the FA in the splenium and stuttering severity in adults who stutter (unpublished study; the results were presented at the 2014 ASHA Convention).

A further finding by Chow and Chang (in press) which distinguished the persistent from the recovered group of stuttering children is an initially higher FA value and an abnormal developmental trajectory in the thalamic radiation (see Fig. 2, Cluster 8, 9, and 10 in the study). These findings as well can hardly be explained as a consequence of stuttering. As the thalamus plays a central role in attention regulation, the findings may be related to an abnormal development of the attention system, possibly increasing the imbalance described above as the causal Factor 1. This assumption is supported by findings of anomalous, mainly decreased functional connectivity between Dorsal as well as Ventral Attention Network and Default Mode Network especially in children who eventually persisted in stuttering (Fig. 3 in Chang et al., 2018).

The hypothesis that transient and persistent developmental stuttering are in core the same disorder, and  that persistence is caused by an additional factor has already been proposed by Ambrose, Cox, and Yairi (1997) in a study of the genetic basis of persistence and recovery. They wrote: “ It was found that recovery or persistence is indeed transmitted, and further, that recovery does not appear to be a genetically milder form of stuttering, nor do the two types of stuttering appear to be genetically independent disorders. Data are most consistent with the hypothesis that persistent and recovered stuttering possess a common genetic etiology, and that persistence is, in part, due to additional genetic factors.”

The proportion of the two factors may differ between individuals, however, Factor 2 seems to be necessary for stuttering to become persistent. Factor 1 may be differently caused in persistent stuttering than in transient stuttering – as mentioned above, the clusters of reduced FA in the arcuate fasciculus (Cluster 1 and 2 in Fig. 1 in Chow and Chang, in press) were larger and the FA value in the anterior cluster was lower in the recovered than in the persistent group. However, in the persisten group, it was found an abnormal, stagnant or downward developmental trajectory of FA in the radiation of the thalamus (Fig. 2, Clusters 8, 9, 10). The thalamus is a part of the brain which plays a central role in the control of attention. We can assume that the male-to-female ratio in persistent stuttering has to do with Factor 1, namely with the fact that hyperactivity and impulsivity are more prevalent in males. 

 

Why are right frontal brain areas overly active?

In this post, I want to discuss the article “Structural connectivity of right frontal hyperactive areas scales with stuttering severity” by Nicole Neef and colleagues, recently published in the journal Brain – see here(free full text).

I start with the question of whether my theory is consistent with the results of the study. After that, I discuss the authors’ hypothesis that stuttering could be caused by a global response suppression mechanism. I use the following abbreviations: BG = basal ganglia, IFG = inferior frontal gyrus, MFG = middle frontal gyrus, SLF = superior longitudinal fasciculus, SMA = supplementary motor area, STG = superior temporal gyrus

Reduced fractional anisotropy in the SLF – related to deficient myelination?

In the left SLF/arcuate fasciculus of the stuttering participants, a weaker connectivity than in controls was found along the major diffusion direction of the fiber tracts. The authors conclude that this “favours the view that atypical structures are insufficiently myelinated or that the axonal packing is reduced therein”. This is consistent with my assumptions about the role of myelination in Section 4.1. However, I don’t believe that the structural deficits in the fiber tracts compromise signal transfer. 

 

If it was the case, and if that caused stuttering, then the disorder could hardly be as variable as it is. It could hardly be so much influenceable by situations, emotions, or anticipations; it could not suddenly be eliminated by conditions like chorus reading. We would expect stuttering to be a more invariable, only gradually changing disorder if it was immediately caused by a structural deficit.

However, there’s an alternative explanation: The fibers are able to work well, and their structural weakness is the result of reduced activation due to a habitual misallocation of attention, i.e., a misallocation of perceptual and processing capacity during speech, and perhaps during other automatic motor behavior (see Section 4.1). 

This view is supported by the evidence that fiber structure develops with training, i.e., depending on activation (e.g., Keller and Just, 2009; Scholz et al,2009), by the evidence of deficient attention regulation in stutterers (see 3.3.1), and by the fact that their auditory areas were often found to be deactivated during stuttered speech (see Table 1), suggesting that auditory feedback is insufficiently involved.

Compensation via uncinate fasciculus 

 

A negative correlation was found between the severity of stuttering and the connection strength (connection probability density) in the right uncinate fasciculus linking the frontal pole to higher-order auditory and multisensory areas of the STG. This finding is consistent with my assumption that an insufficient involvement of auditory feedback plays a crucial role in stuttering. But why is compensated for that deficit by the right uncinate fasciculus being additionally involved?

In Section 3.2, I report some findings suggesting that reduced auditory attention results in a shift of processing from the left more to the right brain hemisphere, and in Section 4.4, I develop a hypothesis based on the dual steam model, why semantically and syntactically correct speech can be produced with little auditory attention, reduced involvement of the SLF, reduced phonological feedback processing, depending more on the ventral stream part of which is uncinate fasciculus.

Is global response suppression the cause of stuttering?

 

Right posterior IFG and right MFG were found to be hyperactive during vocal imagination tasks (imagine speaking versus imagine humming a melody), and the connection strength in some fiber tracts originating from these hyperactive areas was positively correlated with stuttering severity. It is not clear whether these abnormalities are related to the cause of stuttering or to maladaptation or compensation, and the authors hypothesize “that stuttering might be caused by an overly active global response suppression mechanism mediated via the subthalamic nucleus-right IFG-basal ganglia hyperdirect pathway”.They assume that such a global response suppression mechanism “induces an unspecific broad inhibition” which “would hinder the smooth successive execution of appropriate motor actions”.

I think there are some arguments against this hypothesis. First, the subthalamic nucleus-right IFG-BG hyperdirect pathway (via which the global response suppression mechanism is mediated) seems to control voluntary behavior (after the model proposed by Goldberg, 1985). Likewise, right MFG and posterior IFG seem to control mainly voluntary behavior, namely “involved in the ability to apply executive control over actions”. In stuttering, by contrast, speech flow is disrupted against the person’s will.

Secondly, the question would arise why the assumed overactive global suppression mechanism only affects speaking, but not other motor behavior. If the hypothesis was true, it would mean that a neuronal network responsible for the smooth execution of all voluntary movement would completely fail many times a day – but strangely in speaking only.

A third argument against the above hypothesis is provided by cases in which persistent stuttering suddenly and completely disappeared after a lesion in the left hemisphere of the cerebellum (e.g., Bakheit, 2011; see also Section2.1) The crucial role the cerebellum plays in stuttering became clear in the study by Wymbs et al., 2013: They found little across-subject agreement of activated brain regions during stuttered speech – the only region which was overly active in all the four participants was the left cerebellum. Therefore, I think the left cerebellum is the likeliest candidate for the source of signals disrupting speech flow, not least because the cerebellum is involved in the response to errors in motor sequences (e.g, Zheng et al, 2013; see also footnotein Section 2.1).

What role may right SMA and BG play in stuttering?

If greater activation in the right IFG and MFG in the stuttering participants during the imagination tasks was related to the stop response, then perhaps because it was some more difficult for them to suddenly stop when the signal was displayed (I participated in the study myself, and I remember I needed some effort to stop when I just was in the flow in internally humming the melody). Such difficulty in inhibitory control seems to be rather typical of stutterers, as well as a tendency towards hyperactivity and impulsivity (see Section 3.3.1). However, I don’t believe that it immediately causes stuttering; it may rather be (i) a factor in the predisposition for stuttering and (ii) a factor influencing the severity of individual symptoms.

The first assumption – that an overly active SMA-BG circuit contributes to the predisposition for stuttering – is derived from the findings regarding a tendency towards hyperactivity, impulsivity, difficulty in attention regulation (shift of attention, dividing attention in dual tasks), and deficient inhibitory control. All this suggests an imbalance to the favor of voluntary, internally initiated, targeted action, but to the detriment of (non-targeted) perception and response, including the processing and involvement of sensory feedback – processes which are not voluntary but more unconscious and automatic. Likewise, the positive correlation between stuttering severity and the anatomical connections of the right frontal aslant tract linking the posterior IFG with SMA and preSMA may be related to a tendency towards too much control by the will

Background of the second assumption – that an overly active SMA-BG circuit contributes to the severity of symptoms – is the model that a stuttering event consists of two parts: (a) blockage of a motor program, (b) the speaker’s will to continue, that is, the ‘drive’ – the SMA-BG circuit starts the motor program again and again or keeps it active despite its execution is blocked (see also footnote in Section 2.1).

Since the SMA-BG circuit is responsible for voluntary behavior, its activity is influenceable by the will: In stuttering modification therapy, clients learn to give up the urge to speak when feeling a blockage. Overt symptoms or at least their severity can be reduced in this way, hard blocks, long prolongations, or often repeated iterations are avoided. Dopamine receptor blockers seem to act in a similar direction, as Alm (2004) concludes from the literature: the drug “exerts its main effect in reducing superfluous motor activation during stuttering, not in reducing the number of disruptions” (p. 337).

A third role of right frontal brain areas in stuttering must be mentioned for the sake of completeness: volitional control of speech, particularly deliberate speech planning in order to avoid or postpone words feared to be stuttered. Overactivation in the right frontal operculum, negatively correlated with stuttering severity but reduced after successful therapy, may be related to such compensatory behavioral habits.

DAF, stuttering, and central auditory processing

The study I want to discuss in this post is again about the effect of delayed auditory feedback (DAF) on stuttering. Luana Picoloto and her colleagues investigated the “Effect of delayed auditory feedback on stuttering with and without central auditory processing disorders.” The study was recently published in the Journal CoDAS – see here (free full text).

In the study, the fluency-enhancing effect of DAF (100ms delay) in two groups of individuals who stutter was compared: (i) a grroup without central auditory processing disorder (APD) and (ii) a group with APD. It came out that the DAF caused a statistically significant reduction of stuttering frequency in the group without APD, but not in the group with APD.

The reduction of the number of blocks and of repetitions of monosyllabic words was statistically significant in the group without APD. By contrast, in the group with APD, the DAF did not cause statistically significant effects, but there was a tendency towards heightened disfluency, particularly regarding part-word repetitions and prolongations (see Figures 1 and 2 in the paper).

There were also similarities between the groups: The number of blocks was reduced by DAF also in the group with APD, but the reduction did not reach statistical significance. Further, the number of intrusions was tendentially greater with DAF than with natural auditory feedback in both groups.

In their paper, the authors do not speculate about the way in which DAF reduces stuttering. But that’s an important question; I think, to understand the mechanism in which altered auditory feedback reduces stuttering is to understand the pathomechanism of the disorder.

My own hypothesis is: Altered auditory feedback (as long as it is unaccustomed) draws the speaker’s attention to the auditory channel, which improves the processing of auditory feedback and its involvement in speech control (see Section 3.1 on my theory website).

Basis of this hypothesis is the assumption that subtle deficits in central auditory processing cause individuals who stutter to turn away their attention from the auditory channel in order to prevent acoustic overstimulation. The core of the auditory processing deficit seems to be a less effective auditory gating, that is, the processing of redundant acoustic input is insufficiently suppressed (see Kikuchiet al., 2011).

Children with such an auditory processing deficit may early develop a compensatory habit of attentional misallocation, namely to always turn attention away from the auditory channel, except moments of active listening. Altered auditory feedback overcomes this habit because (and as long as) it sounds unfamiliar and odd. This hypothesis is supported by the fact that devices like SpeechEasy reduce stuttering even when delay and frequency shift are disabled (Foundas et al., 2013; Unger, Glück, and Cholewa, 2012). Thus it seems not to be the delay or the frequency shift as such which acts, but the simple fact that it sounds anyway odd.

Is my theory consistent with the new findings obtained by Picoloto and colleagues? The first point is: Can my theory be true given that many stutterers have no (diagnosed) APD? There are two possible answers: (i) Deficits in central auditory processing may be very subtle in many a stutterer such that the scores in standardized tests are within normal range. (ii) All the tests applied for diagnosing APD (see Procedures) aim to detect something presented and not heard, but the problem of some stutterers may be that they hear too much too intensively because of a deficient auditory gating (see above).

An alternative possibility is: There are two groups in persistent stuttering, both with a deficit in attention control, but with versus without APD. I assume this because I don’t believe that APD immediately causes stuttering. If that was the case, then the disorder could not be as influenceable by emotions, situations, anticipations as it is. I think attention (i.e., the allocation of perceptual and processing capacity) is the interface between the mechanism of stuttering (which immediately causes the symptoms) and factors that negatively impact attention control, among them APD, but also fear or adverse communication situations.

A second point is: When I (i) assume that APD causes a misallocation of attention during speech, and this, in turn, causes stuttering (see Chapter 2 of my website),and when I (ii) assume that DAF overcomes the misallocation of attention, then one may expect a stronger (or at least a similar) effect of DAF in the group with APD, but the contrary was found. A possible explanation may be that the delay of 100ms was too much for the group with APD. In earlier studies. good effects were achieved with delays of 50ms and 75ms, and, as mentioned above, even with an active device in the ear, but without feedback alteration. On the other hand, a too long delay evokes disfluencies not only in nonstutterers, but also in stutterers. The increased number of intrusions perhaps indicates that the DAF was irritating for at least some participants in both groups.

If so, then we can assume that some participants attempted to ignore the DAF, that is, they all the more turned their attention away from the auditory channel, which, after my theory, results in more stuttering. And it would not be surprising if those with APD were more apt to behave in this way. They may be acoustically more sensitive and may more likely experience a 100ms delay as annoying.

If my assumption is true that the DAF effect on stuttering is an effect on attention, then there are always two possibilities: (i) the appropriate delay draws attention to the auditory channel and reduces stuttering, and (ii) an inappropriate, i.e., too long delay increases the person’s disposition to ignore the auditory channel, which can increase stuttering. The crucial thing is: Delayed auditory feedback must still be useful for the (automatic and unconscious) self monitoring of speech and for the mechanism of ‘audiophonatorycoupling’, which is not the case when the delay is too long. Therefore, it may be interesting to test the effect of various delays in a further study, or the effect of delays individually adapted.

The mystery of the DAF effect on stuttering

My theory website on stuttering has been online for two years now. In that time I added many paragraphs and footnotes in order to include new empirical results, thus the text on the pages has become longer and longer, and if I continue in this way, then it may become confusing. Therefore I start this blog to discuss new papers on stuttering here. I will do this in the context of the theory published on my website: Are the assumptions in the theory consistent with new results of empirical research? Does the theory help to explain new empirical results? By that, I hope, I can a little bit contribute to the discussion about the causes of stuttering.
 

The first article I want to discuss is "Stuttering adults’ lack of pre-speech auditory modulation normalizes when speaking with delayed auditory feedback." by Ayoub Daliri and Ludo Max. The study was recently published in the journal Cortex, see here (free full text).

The main findings, in my view, are:

(1) The function of pre-speech auditory modulation is probably not a suppression of auditory input during speech (as was assumed earlier), but rather an optimization of the processing of auditory feedback.

(2) Pre-speech auditory modulation was limited in adults who stutter compared with control participants. Figure 5 shows that the reduction of the N1 amplitude (indicating pre-speech auditory modulation) in all stuttering participants was smaller than the smallest reduction in the non-stuttering control group.

(3) Delayed auditory feedback (DAF) caused an increase of pre-speech auditory modulation in most of the stuttering participants, such that it was similar on average to that in the control group. The authors write that in adults who stutter, “DAF paradoxically tends to normalize their otherwise limited pre-speech auditory modulation.”

The results are very important because they first time shed a light on the mechanism how DAF works when reducing stuttering: It supports pre-speech auditory modulation and (probably) the processing of auditory feedback and its integration in speech control. The understanding in which way DAF reduces the disorder, should help us to better understand the disorder itself.

In Section 3.1 on my website, I assume that DAF and other kinds of altered auditory feedback work in the way that they draw the speaker’s attention to the auditory channel, at least as long as the feedback alteration is experienced as unaccustomed. Is that assumption consistent with the new findings?

I think it is. In the study (Experiment 2), pre-speech auditory modulation was measured as the attenuation of the amplitude of the N1 component of an auditory-evoked potential. The potential was elicited by a probe tone presented ca. 200ms prior to (a) silent reading and (b) reading aloud. With normal auditory feedback (NAF), the N1 amplitude in the control group was reduced prior to reading aloud versus silent reading, but there was no such difference in the stuttering group. To put it crudely, the stuttering participants (or their brains) behaved as if they did not expect anything to hear at speech onset.

Auditory N1 is weaker after standard stimuli, but stronger after a deviant stimulus. It is also weaker when a person controls the creation of auditory stimuli as it is the case at speech onset, but also when the person elicits a computer sound by pushing a button – the N1 is stronger when the sound is started by the computer (see Behroozmand &Larson, 2011, for an overview). This together strongly suggests that N1 has to do with expectation: It is stronger after an unexpected stimulus, but weaker after an expected stimulus.

And now, I think there is a relationship (an interaction) between expectation and attention: Someone expecting a sound will probably listen, and someone listening will probably expect to hear something. When a person’s attention is directed to the auditory channel, and he or she expects something to hear, then the N1 amplitude after a probe tone will be smaller than in a situation in which no attention is directed to the auditory channel such that the probe tone is more surprising.

Possibly, N1 reflects a brain mechanism which controls selective attention on the basis of sensory input in a way that attention is primarily drawn to new or unexpected things – a mechanism that certainly proved beneficial for survival in the course of the evolution.

If so, we can interpret pre-speech auditory modulation as a modulation of attention: In normal speakers, some attention is directed to the auditory channel prior to and during speech such that auditory feedback is properly processed (verbal input is poorly processed without attention to the auditory channel; see, e.g., Sabri et al., 2008).

In persons who stutter, this pre-speech modulation of attention is weaker or absent, but DAF draws their attention to the auditory channel because it sounds odd. Hence I think it is not paradoxical that DAF normalizes pre-speech auditory modulation in stutterers.

However, that was not the case in all of the stuttering participants in the study. Figure 4E shows that DAF increased the amount of N1 modulation only in 9 of 12 stuttering subjects – and even in only 4 of 12 control subjects. Is that consistent with the assumption DAF modulates attention?

One possible reason for the different response to DAF in the stuttering group may be that some participants experienced a delay of 100ms as unpleasant such that they strove to ignore it. In the SpeechEasy device, the manufacturer’s default setting is a delay of 60ms (Foundas et al., 2013), the two devices tested by Unger, Glück,and Cholewa (2012) had a delay of 50ms as default setting. Antipovaet al. (2008) found delays of 50ms and 75ms to be effective. Hence, a delay of 100ms may have been too long for some individuals. In a future replication of Experiment 2, the effect of various delays should be tested.

But why did the DAF reduce the amount of pre-speech auditory modulation in the majority of the control participants? I think it was the same as with the three stutterers: They experienced the DAF as annoying and strove to ignore the auditory channel. Why did much more nonstutterers than stutterers behave in this way? A possible answer is: Since the natural auditory feedback of speech is optimally processed in normal speakers, they experience a feedback delay of 100ms more likely as a disturbance than stutterers do.

In sum, I think the exciting new results obtained by Daliri and Max are consistent with the assumption that DAF and other kinds of feedback alteration (like chorus reading, whispering, speaking in an assumed voice) reduce stuttering by drawing the speaker’s attention to the auditory channel.

The uneven response to frequency-altered auditory feedback in the stuttering group in Experiment 1 may again result from different subjective experience: Perhaps, some of the stuttering participants did not perceive the higher pitch as unpleasant, thus they did not compensate for (some stutterers report they perceive their own voice - with natural feedback - as unpleasant or droning).

The negative correlation between the response to frequency-altered feedback in Experiment 1 and the amount of pre-speech auditory modulation with natural auditory feedback in Experiment 2 (Figure 5) is really astonishing. It does not look like chance, but I have no idea what it could mean. No end of mystery...