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
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 Section 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.
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.
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 Section 2.1) 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 the footnote in Section 2.1).
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 the in 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.
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