Effects of generation mode in fMRI adaptations of semantic fluency: paced production and overt speech

Abstract

Verbal fluency is a widely used neuropsychological paradigm. In fMRI implementations, conventional unpaced (self-paced) versions are suboptimal due to uncontrolled timing of responses, and overt responses carry the risk of motion artifact. We investigated the behavioral and neurofunctional effects of response pacing and overt speech in semantic category-driven word generation. Twelve right-handed adults (8 females), ages 21-37 were scanned in four conditions each: paced-overt, paced-covert, unpaced-overt, and unpaced-covert. There was no significant difference in the number of exemplars generated between overt versions of the paced and unpaced conditions. Imaging results for category-driven word generation overall showed left-hemispheric activation in inferior frontal cortex, premotor cortex, cingulate gyrus, thalamus, and basal ganglia. Direct comparison of generation modes revealed significantly greater activation for the paced compared to unpaced conditions in right superior temporal, bilateral middle frontal, and bilateral anterior cingulate cortex, including regions associated with sustained attention, motor planning, and response inhibition. Covert (compared to overt) conditions showed significantly greater effects in right parietal and anterior cingulate, as well as left middle temporal and superior frontal regions. We conclude that paced overt paradigms are useful adaptations of conventional semantic fluency in fMRI, given their superiority with regard to control over and monitoring of behavioral responses. However, response pacing is associated with additional non-linguistic effects related to response inhibition, motor preparation, and sustained attention.

Fig. 1

Mean number of exemplars generated by each of subjects in the paced overt (solid) and unpaced overt (hatched) conditions. Error bars are standard error of the mean. The inserted p-values result from 2-tailed t-tests performed for each subject comparing exemplars generated in four paced versus four unpaced blocks.

Fig. 2

Mean deviation in head position for each of the four generation modes, collapsed across twelve subjects and six movement directions (translation and rotation in the x, y, and z planes). Error bars are standard error of the mean.

Fig. 3

T-maps showing clusters of significant activation for (A) word generation overall, collapsed across generation modes. Effects associated with Response Pacing are shown in (B) for Paced and Unpaced conditions and for the direct comparison between Paced and Unpaced conditions (C), which yielded greater activity in Paced conditions (but no inverse effects). Effects associated with Response Mode are seen in (D) for the Overt and Covert conditions and the direct comparison between the two modes (E), which resulted exclusively in greater effects for the Covert conditions.