The Effect of Speech Repetition Rate on Neural Activation in Healthy Adults: Implications for Treatment of Aphasia and Other Fluency Disorders

Abstract

Functional imaging studies have provided insight into the effect of rate on production of syllables, pseudowords, and naturalistic speech, but the influence of rate on repetition of commonly-used words/phrases suitable for therapeutic use merits closer examination.Aim: To identify speech-motor regions responsive to rate and test the hypothesis that those regions would provide greater support as rates increase, we used an overt speech repetition task and functional magnetic resonance imaging (fMRI) to capture rate-modulated activation within speech-motor regions and determine whether modulations occur linearly and/or show hemispheric preference.Methods: Twelve healthy, right-handed adults participated in an fMRI task requiring overt repetition of commonly-used words/phrases at rates of 1, 2, and 3 syllables/second (syll./sec.).Results: Across all rates, bilateral activation was found both in ventral portions of primary sensorimotor cortex and middle and superior temporal regions. A repeated measures analysis of variance with pairwise comparisons revealed an overall difference between rates in temporal lobe regions of interest (ROIs) bilaterally (p < 0.001); all six comparisons reached significance (p < 0.05). Five of the six were highly significant (p < 0.008), while the left-hemisphere 2- vs. 3-syll./sec. comparison, though still significant, was less robust (p = 0.037). Temporal ROI mean beta-values increased linearly across the three rates bilaterally. Significant rate effects observed in the temporal lobes were slightly more pronounced in the right-hemisphere. No significant overall rate differences were seen in sensorimotor ROIs, nor was there a clear hemispheric effect.Conclusion: Linear effects in superior temporal ROIs suggest that sensory feedback corresponds directly to task demands. The lesser degree of significance in left-hemisphere activation at the faster, closer-to-normal rate may represent an increase in neural efficiency (and therefore, decreased demand) when the task so closely approximates a highly-practiced function. The presence of significant bilateral activation during overt repetition of words/phrases at all three rates suggests that repetition-based speech production may draw support from either or both hemispheres. This bihemispheric redundancy in regions associated with speech-motor control and their sensitivity to changes in rate may play an important role in interventions for nonfluent aphasia and other fluency disorders, particularly when right-hemisphere structures are the sole remaining pathway for production of meaningful speech.

Brain activation during non-habitual speech production: Revisiting the effects of simulated disfluencies in fluent speakers

“…This was somewhat surprising, because if the observed activation increases were indeed associated with the effort and attention required to produce atypical speech, similar patterns of increased activation were expected to occur in the control participants. This interpretation is further supported by the findings on speech rate changes and fluency-inducing conditions in fluent speakers discussed above [3,11,17,18]. One of the potential explanations for this unexpected finding discussed in the De Nil et al [19] paper was that activation changes in the fluent speakers may have been less pronounced and remained sub-threshold because of methodological reasons (use of a lower field strength (1.5T) scanner, sparse scanning, and use of auditory stimuli).…”

“…Brain imaging studies of fluent speakers have greatly advanced our knowledge of the brain areas involved in speech production [1][2][3][4][5]. Combined, these studies have shown that speech production is supported by a network of brain areas that includes the pre-and postcentral gyri, posterior inferior frontal gyri, medial and lateral premotor cortex, anterior insula, superior temporal gyri, posterior planum temporale region, basal ganglia and cerebellum [4].…”

“…The authors observed a linear change in BOLD response in speech-related brain regions including the supplementary motor area, the left anterior insula, bilateral thalamus, bilateral sensorimotor cortex, cerebellum and basal ganglia, when fluent-speaking adults were asked to speak at three different self-generated syllable rates. More recently, Marchina and colleagues [3] studied the effect of speech repetition rate on neural activation in 12 healthy controls to identify regions that can support recovery from speech disorders and to aid the development of adaptive treatment protocols for non-fluent aphasia, dysarthria, apraxia of speech and stuttering. They observed a significant linear increase in activation in the bilateral superior temporal areas with self-generated speech rate changes, suggesting that sensory feedback corresponds directly to task demands.…”

Even when right is all that's left: There are still more options for recovery from aphasia

“…Two prominent hypotheses inform our current understanding of how the brain recovers speech‐motor function after an insult: (1) Recruitment of perilesional cortex to form a new network of regions in the affected hemisphere (the perilesional hypothesis), (2) engagement of homotopic regions and associated fiber tracts in the undamaged hemisphere to facilitate recovery of speech‐motor function, and (3) a combination of both. The “right‐shift hypothesis” is based on the neural redundancy theory that both hemispheres have the capacity to support speech‐motor function, although the degree to which the right hemisphere becomes involved after damage to the left may differ from person to person and/or depend upon factors that are not yet fully understood. Among the potential determinants of which route is chosen and which leads to success, size and site of left‐hemisphere lesions and lesion load of the arcuate fasciculus (AF) or other speech/language‐relevant structures, may be the most important.…”

“…Whether or not recruitment of the right hemisphere (1) is a sign of “incomplete recovery” or “less effective compensation,”, (2) occurs only as a transient phenomenon during the recovery process, or (3) indicates use of built‐in redundancy to facilitate recovery in case of an insult to the left hemisphere is still a matter of debate.…”