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.
Highlights
IntroductionFluent speech production involves a series of integrated commands [e.g., predictive commands to the motor cortex to establish a target (feedforward); assessment/analysis commands to auditory-motor regions to evaluate accuracy of output compared to the predicted target (feedback); and when a mismatch is detected, corrective commands to motor cortices to both initiate and respond to those auditory targets in the feedforward/feedback loop (modification/correction)] (Houde and Jordan, 1998; Tourville et al, 2008; Houde and Nagarajan, 2011)
In healthy individuals, fluent speech production involves a series of integrated commands [e.g., predictive commands to the motor cortex to establish a target; assessment/analysis commands to auditory-motor regions to evaluate accuracy of output compared to the predicted target; and when a mismatch is detected, corrective commands to motor cortices to both initiate and respond to those auditory targets in the feedforward/feedback loop] (Houde and Jordan, 1998; Tourville et al, 2008; Houde and Nagarajan, 2011)
The linear effects seen in superior temporal lobe region of interest (ROI) suggest that sensory feedback corresponds directly to task demands
Summary
Fluent speech production involves a series of integrated commands [e.g., predictive commands to the motor cortex to establish a target (feedforward); assessment/analysis commands to auditory-motor regions to evaluate accuracy of output compared to the predicted target (feedback); and when a mismatch is detected, corrective commands to motor cortices to both initiate and respond to those auditory targets in the feedforward/feedback loop (modification/correction)] (Houde and Jordan, 1998; Tourville et al, 2008; Houde and Nagarajan, 2011). Palmer et al (2001) showed similar activation patterns for both response modes once motor activity associated with overt speech was removed; others found distinctly different patterns of neural activation for covert and overt speech Both Huang et al (2002) and Shuster and Lemieux (2005) observed stronger activation for overt speech than for covert speech; Brumberg et al (2016) noted that speech output intensity led to better identification of neural correlates for overt, but not covert sentence production; and Basho et al (2007) suggested that without overtly spoken responses, the scope of language tasks for functional magnetic resonance imaging (fMRI) would be limited by the inability to assess subjects’ participation, obtain behavioral measures, or monitor responses. Overt repetition of real words is important for studies of speech repetition rate because it enables continuous monitoring of task compliance and accuracy of responses/consistency of adherence to rate within and across subjects
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