Altered Modulation of Silent Period in Tongue Motor Cortex of Persistent Developmental Stuttering in Relation to Stuttering Severity

Abstract

Motor balance in developmental stuttering (DS) was investigated with Transcranial Magnetic Stimulation (TMS), with the aim to define novel neural markers of persistent DS in adulthood. Eleven DS adult males were evaluated with TMS on tongue primary motor cortex, compared to 15 matched fluent speakers, in a "state" condition (i.e. stutterers vs. fluent speakers, no overt stuttering). Motor and silent period thresholds (SPT), recruitment curves, and silent period durations were acquired by recording tongue motor evoked potentials. Tongue silent period duration was increased in DS, especially in the left hemisphere (P<0.05; Hedge's g or Cohen's dunbiased = 1.054, i.e. large effect size), suggesting a "state" condition of higher intracortical inhibition in left motor cortex networks. Differences in motor thresholds (different excitatory/inhibitory ratios in DS) were evident, as well as significant differences in SPT. In fluent speakers, the left hemisphere may be marginally more excitable than the right one in motor thresholds at lower muscular activation, while active motor thresholds and SPT were higher in the left hemisphere of DS with respect to the right one, resulting also in a positive correlation with stuttering severity. Pre-TMS electromyography data gave overlapping evidence. Findings suggest the existence of a complex intracortical balance in DS tongue primary motor cortex, with a particular interplay between excitatory and inhibitory mechanisms, also in neural substrates related to silent periods. Findings are discussed with respect to functional and structural impairments in stuttering, and are also proposed as novel neural markers of a stuttering "state" in persistent DS, helping to define more focused treatments (e.g. neuro-modulation).

Fig 1. Motor thresholds in the stuttering and fluent speakers groups.

Data obtained for MT, AMT, and SPT are reported for DS and fluent speakers. Statistically significant comparisons are indicated with an asterisk, while marginally significant comparisons are indicated with a circle.

Fig 2. Silent period durations obtained in the stuttering and fluent speakers groups.

Significant differences are indicated with an asterisk. Data are reported by considering also the right/left side of the tongue. LH = TMS administered on the left hemisphere; RH = TMS administered on the right hemisphere.

Fig 3. Pre-TMS EMG data obtained in the two groups during sustained tongue contractions requested for the silent period TMS protocol.

About 60–70% of maximal muscular activation was requested. Marginally significant comparisons are indicated with a circle. Data are reported by considering also the right/left side of the tongue. LH = TMS administered on the left hemisphere; RH = TMS administered on the right hemisphere.

Fig 4. Significant correlations between TMS data and stuttering severity.

Main significant findings obtained from correlation analyses between SSI-4, BigCAT, and TMS are reported. Participants are reported on the x-axis. Positive correlation between SSI-4 and BigCAT in DS are reported in (A); positive correlation between SSI-4, tongue AMT and SPT (obtained when stimulating the left hemisphere) in stuttering are reported in (B); positive correlation between SSI-4 and silent period durations, obtained from the right FDI muscle when stimulating the left hemisphere motor cortex in DS are reported in (C); positive relation between BigCAT and silent period durations recorded from tongue muscles (left/right side) when stimulating the left hemisphere motor cortex in all participants, is reported in (D).