Besides the question of whether the structural deficits in the left superior longitudinal fasciculus (SLF) cause stuttering (symptoms), another question is of interest: Do these deficits play any role in the outbreak of stuttering in childhood? In this case, the deficits ought to be already detectable in young children, close to the onset of stuttering.
The first examination of white matter tracts in children who stutter was carried out by Chang et al. (2008). Participants were right-handed boys between 9 and 12 years of age, namely eight with persistent stuttering, seven who had recovered, but had stuttered for 2–3 years prior to recovery, and seven normal fluent boys (control group). The boys with persistent stuttering might have stuttered also for some years prior to the examination; the exact duration is not told.
In the stuttering as well as in the recovered groups, reduced fractional anisotropy (FA) in the left SLF was found, similar to the findings of Sommer et al. (2002). However, in the recovered group. the deficit was smaller, and a greater fractional anisotropy was found in the right SLF, compared to both the other groups (see Fig. 6 in Chang et al., 2008). Even if the latter differences were not statistically significant. they suggest that the deficits in fiber maturation, in part, had settled in the recovered children, and in part, they had been compensated in the right hemisphere.
Maybe the boys who recovered from stuttering had learned to better allocate their attention during speech, thus more perceptual- and processing capacity remained for auditory feedback. If the processing of auditory feedback and the involvement of this information in speech control was partially shifted to the right hemisphere, the reason may be that attention allocation was not yet well automatized in some of these children. A further possibility is that they directed attention more to the sound aspect or the prosody of their own speech Unfortunately, we have no data of adults who recovered from stuttering, thus we don’t know if the right-shift disappears with time.
The lower FA in the 9–12-year-old stuttering children can be the result of a longstanding misallocation of attention during speech (see last section). But what about young stuttering children near the onset of the disorder? Chang and Zhu (2013), Chang, Zhu, Choo, and Angstadt (2015), and Chow and Chang (2017) investigated the white matter development in of young children (3 – 9, 10, or 12 years of age, resp., mean age 6 ½ years). They compared three groups: those who later persisted in stuttering, those who later recovered from the disorder, and normal fluent controls.
The stuttering children showed structural and functional abnormalities in several brain regions, among them in the connection between auditory, premotor and motor areas of the cortex as well as in the connection between cortical and subcortical regions (basal ganglia, cerebellum, and others), and in the corpus callosum. Let us furst look at the findings concerning the connection between the region of speech perception and the region of speech control – roughly said, between Wernicke’s and Broca’s areas. The question is: Are the structural deficits in the left SLF that were found in adult stutterers, in older stuttering children, and even, albeit in a lower degree, in recovered children also significant in young stuttering children?
By means of probabilistic tractography, Chang and Zhu (2013) did not find significant group differences in the left SLF between stuttering children and controls. Chang, Zhu, Choo, and Angstadt (2015), by means of voxel-based diffusion tensor imaging and with more participants, found similar structural deficits in the left SLF as was previously found in adults and older children who stutter. However, these findings can still be interpreted as a consequence or concomitant of stuttering (read more).
In sum, the onset of childhood stuttering seems to be related to certain structural deficits in the left SLF / arcuate fasciculus, possibly the result of delayed fiber maturation prior to the onset of stuttering. This may be due to a reduced involvement of sensory feedback in speech control or in motor control in general, resulting from an imbalance in the automatic, i.e., involuntary and unconscious allocation of attention, i.e., of perceptual and processing capacity. That means, these deficits in the left SLF indicate a risk of stuttering, mainly of transient stuttering with subsequent recovery. Other structural deficits in the left SLF seem to reflect the development of persistent stuttering. However, in both cases, I do not assume that the structural deficits immediately cause stuttering symptoms.
Another finding may be closer related to the outbreak of the disorder: Chang and Zhu (2013) found that the stuttering children, as a group, had a structural deficit (reduced FA) in a tract interconnecting the left pars opercularis with the posterior temporal region through a ventrally located tract through the extreme capsule fiber system (ECFS). Chang, Zhu, Choo, and Angstadt (2015) also found reduced FA in the left extreme capsule in the stuttering children, with anisotropy values being negatively correlated with stuttering severity (read more).
Figure 14:Charting of the SLF (as in Fig. 13) and the tract of the extreme capsule fiber system (ECFS) on the left brain hemisphere (for more details, compare Fig. 8 in Frey et al. (2008), Fig. 1 in Friederici (2012), Fig. 6 in Kelly et al. (2010)); aSTG / pSTG = anterior / posterior superior temporal gyrus.
A structural deficit in the ECFS was not found in adults or in older children who stutter (sue, e.g., Cai et al., 2014b; Kronfeld-Duenias et al., 2016). Possibly, these deficits exist only at (and a time after) the onset of childhood stuttering and gradually disappear in the course of further development not only in those who recover, but also in persistent stutterers. However, Chow and Chang (2017) do not report group differences in the ECFS in young children; hence further research may clarify this issue.
The most interesting finding in the study by Chow and Chang (2017), in my view. is Cluster 4 in the splenium of the corpus callosum (Fig. 1 in the paper). The diagram shows lower FA in the persistent group, compared to both recovered children and controls (who range equally in this cluster). The difference is great already with the youngest children, and there is no much overlap between the persistent group and the recovered+control group, therefore, it can hardly be a consequence of stuttering, a compensation, or the like. 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 DTI study; the results were presented at the 2014 ASHA Convention)
The affected fibers of the splenium probably connect bilateral temporal regions (comp. Kuvazeva, 2013), and the lower FA in the persistent group may be related to a less effective labor division between hemispheres in auditory processing. This assumption is supported by the many findings suggesting a subtle auditory processing disorder in persistent stuttering as well as with findings of reduced temporal, but also cochlear lateralization in the processing of verbal stimuli (see Section 3.3.2).
A further brain region where FA differed between the persistent group, on the one hand, and the recovered and control group, on the other hand, is the thalamic radiation (Clusters 8-10, Fig. 2 in the paper). Here, however, the FA value in the persistent group, also in the youngest children, is tendentially above that of the other groups and stagnates or decreases with age. These fibers connect the thalamus with motor regions as well as with prefrontal regions, and higher FA values could here indicate a more intensive interaction of the thalamic attention system (Wimmer et al., 2015) with cognition and motor planning, possibly to the detriment of the involvement of perception in behavioral control – in other words, an attentional bias more to planned, internally initiated action than to perception-based reaction or, in short, an imbalance between action and perception (comp. Section 3.3.1).
However, the scatter plots (upper row in Fig. 2 in Chang et al. (2015)) show that in the left inferior frontal gyrus (BA44) as well as in the left middle temporal gyrus, differences in FA were tendentially smallest between the youngest children and became greater with age, that is, more or less with the duration of stuttering. And there were many more regions in which the group difference in fractional anisotropy (stutterers < controls) was correlated with age (see Table 3 in the paper).
A significant difference between the youngest children of both groups is only in fibers beneath the motor cortex. However, this difference comes about due to the fact that some of the non-stuttering children (8 out of 40) have values higher than the highest value of any stuttering child, and some of the stuttering children (6 out of 37) have values lower than the lowest value of any non-stuttering child – whereas the majority in both groups range similarly. So there may be a subgroup of children who have motor deficits, which could have contributed to the outbreak of their stuttering – however, we don’t know whether the affected fibers beneath the motor cortex have projections in the motor cortex.
Apart from the six children who had very low fractional anisotropy values beneath the motor cortex, the youngest stuttering children hardly differed from their age-matched normal fluent peers in the left SLF. Differences tendentially became greater with age, that is, more or less with the duration of stuttering. This, in my view, does not suggest that structural deficits in the SLF are the cause of stuttering.
The FA in Cluster 1 in the frontoparietal region is in both stuttering groups (those who later persisted and those who later recovered) lower on average than in the control group and in the recovered group lower than in the persistent group. The difference is present also in the youngest children, hence the lower FA in this cluster seems to be related to the onset of stuttering, but not to persistence or recovery. Possibly, the affected fibers play a role in the involvement of sensory feedback (perhaps also of the feedback of breathing movements) in the control of speech.
Cluster 2 is located in the posterior temporal region. Similar to Cluster 1, average FA in both stuttering groups is lower than in the control group, and in the recovered group lower than in the persistent group. The control group as well as the recovered group show a slight decrease of FA with age in this cluster (which may be the normal development), but the persistent group does not. A possible speculation that would explain the somewhat peculiar developmental pattern is: These fibers are involved in self-monitoring and in the detection of errors, the number of which decreases in normal fluent children and in those who recover from stuttering, but not in the persistent group because of invalid error signals.
The FA in Cluster 5 and 6 seems to play no role in the outbreak of childhood stuttering, because the values of the youngest children are similar, and there is much overlap between the groups. The development of FA in both clusters shows a growing difference between the recovering and the persistent group: an increase of FA with age in the first, but a decrease in the second one.
A negative correlation between fractional anisotropy and stuttering severity was found in many other brain regions in which fractional anisotropy was reduced compared to controls (see Table 4 in Chang et al. (2015)). However, these results were driven to a large extent by three of the most severe cases (all boys) within the participant pool. When the three most severe cases were excluded from analysis, only the left extreme capsule and left supramarginal gyrus remained significant in their negative correlation with stuttering severity. The left supramarginal gyrus is a sensory association area probably involved in the integration of sensory feedback in speech control.
Interestingly, only in these two areas (left supramarginal gyrus and left extreme capsule), the negative correlation between fractional anisotropy and stuttering severity was equally evident in boys and girls – in the extreme capsule, the correlation was even more significant in the girls – which suggests that structural deficits in these areas are related to the onset of childhood stuttering since its probability is approximately equal in both sexes.
Since stuttering severity (SSI) includes features that may be more related to secondary behaviors, stuttering frequency might be the measure more related to the cause of the disorder. When stuttering frequency (per cent stuttered utterances /total syllables) rather than stuttering severity (SSI) was entered for correlation analysis with fractional anisotropy, with the three very severely stuttering boys included, only 7 instead of 24 clusters showed significant negative correlation with fractional anisotropy values (bold in Table 4 in Chang et al. (2015)). From the seven clusters, two were located in the cerebellum, two in the left SLF and/or motor/somatosensory cortex, and three in fiber tracts running through the extreme capsule, two of them in the left hemisphere. This also suggests an important role of those fibers in childhood stuttering. About the role of the cerebellum see Section 2.1