Tuesday, January 2, 2018

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.

Saturday, December 16, 2017

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.

Tuesday, November 28, 2017

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...