fMRI reveals two distinct cerebral networks subserving speech motor control

TLDR

Few studies have mapped the cerebral organization of speech motor control or the mechanisms underlying dysarthria after brain lesions. The study aimed to investigate the neural basis of speech motor control using fMRI. Eight healthy volunteers performed syllable repetitions paced by click trains (2–6 Hz) while undergoing fMRI, compared to passive listening. The fMRI data revealed two distinct speech‑motor networks—one involving medial/dorsolateral premotor areas, anterior insula, and superior cerebellum, and another comprising sensorimotor cortex, basal ganglia, and inferior cerebellum—whose activation patterns varied with repetition frequency, supporting separate preparation and execution stages and explaining differential speech rates in Parkinson’s and cerebellar disease.

Abstract

<b>Background:</b> There are few data on the cerebral organization of motor aspects of speech production and the pathomechanisms of dysarthric deficits subsequent to brain lesions and diseases. The authors used fMRI to further examine the neural basis of speech motor control. <b>Methods and Results:</b> In eight healthy volunteers, fMRI was performed during syllable repetitions synchronized to click trains (2 to 6 Hz; vs a passive listening task). Bilateral hemodynamic responses emerged at the level of the mesiofrontal and sensorimotor cortex, putamen/pallidum, thalamus, and cerebellum (two distinct activation spots at either side). In contrast, dorsolateral premotor cortex and anterior insula showed left-sided activation. Calculation of rate/response functions revealed a negative linear relationship between repetition frequency and blood oxygen level–dependent (BOLD) signal change within the striatum, whereas both cerebellar hemispheres exhibited a step-wise increase of activation at ∼3 Hz. Analysis of the temporal dynamics of the BOLD effect found the various cortical and subcortical brain regions engaged in speech motor control to be organized into two separate networks (medial and dorsolateral premotor cortex, anterior insula, and superior cerebellum vs sensorimotor cortex, basal ganglia, and inferior cerebellum). <b>Conclusion:</b> These data provide evidence for two levels of speech motor control bound, most presumably, to motor preparation and execution processes. They also help to explain clinical observations such as an unimpaired or even accelerated speaking rate in Parkinson disease and slowed speech tempo, which does not fall below a rate of 3 Hz, in cerebellar disorders.