Neural systems supporting lexical search guided by letter and semantic category cues: a self-paced overt response fMRI study of verbal fluency

Abstract

Verbal fluency tasks have been widely used to evaluate language and executive control processes in the human brain. FMRI studies of verbal fluency, however, have used either silent word generation (which provides no behavioral measure) or cued generation of single words in order to contend with speech-related motion artifacts. In this study, we use a recently developed paradigm design to investigate the neural correlates of verbal fluency during overt, free recall, word generation so that performance and brain activity could be evaluated under conditions that more closely mirror standard behavioral test demands. We investigated verbal fluency to both letter and category cues in order to evaluate differential involvement of specific frontal and temporal lobe sites as a function of retrieval cue type, as suggested by previous neuropsychological and neuroimaging investigations. In addition, we incorporated both a task switching manipulation and an automatic speech condition in order to modulate the demand placed on executive functions. We found greater activation in the left hemisphere during category and letter fluency tasks, and greater right hemisphere activation during automatic speech. We also found that letter and category fluency tasks were associated with differential involvement of specific regions of the frontal and temporal lobes. These findings provide converging evidence that letter and category fluency performance is dependent on partially distinct neural circuitry. They also provide strong evidence that verbal fluency can be successfully evaluated in the MR environment using overt, self-paced, responses.

Figure 1

Category and letter fluency tasks (C,L) vs. “Months” automatic speech control condition (M). Blue areas indicate regions with a greater activation during the automatic speech; Red areas indicate regions with a greater activation during the fluency tasks. Activations are thresholded at p<0.05 (corrected for multiple comparisons). Bar graphs on right indicate the average signal intensity during each of the 5 tasks, averaged over all subjects and over the region of interest indicated by the number (1–4). (R.STG = Right Superior Temporal Gyrus, R.SMG = Right Supramarginal Gyrus, L.Fus = Left Fusiform Gyrus, L.PrCG/IFG = Left Precentral Gyrus/Inferior Frontal Gyrus.) Note that activation associated with automatic speech is greater in the right hemisphere, whereas activation associated with the fluency tasks is left hemisphere lateralized.

Figure 2

Category vs. Letter Fluency. Regions with greater activation during the category fluency tasks (C) are shown in red, while regions with greater activation during the letter fluency tasks (L) are shown in blue. Activations are thresholded at p<0.05 (corrected for multiple comparisons). Compared to category fluency, letter fluency resulted in greater activation in left precentral/inferior frontal gyrus (a), bilateral ventral occipito-temporal cortex (b), and bilateral superior parietal cortex (c). Category fluency resulted in greater activation in occipital (visual) cortex, fusiform (b), and left middle frontal gyrus (c). Frontal activation with a greater response to category cues (left middle frontal gyrus, yellow arrow) is located superior and anterior to the frontal activation with a greater response to letter cues (left precentral/inferior frontal gyrus, black arrow).

Figure 3

Main effect of task-switching. Regions with greater activation during verbal fluency in response to two categories or letters (2) compared to single category or letter cues (1) are indicated in red. This includes bilateral premotor areas, superior parietal cortex, ventral occipito-temporal cortex, and posterior cingulate. No regions show a greater activation to single category or letter cues (blue).

Figure 4

Latency analysis - Main effect of task vs. fixation: Colored regions show the main effect of the task vs. fixation. The color scale indicates the timing of the signal changes relative to the typical BOLD response. Red = earlier than typical BOLD response (i.e. synchronous with task timing, and indicative of motion); Green = timing similar to typical BOLD response. Signal changes occurring in synchrony with the task (indicated by gray regions in the time series) are visible near the mouth and in the inferior temporal lobe. These motion-induced signal changes occur several seconds before BOLD signal changes in motor and language regions. Time courses from 3 regions are shown on the right. The blue and red curves represent the ideal BOLD and motion induced signal changes, respectively. Signals from the mouth/jaw area and the inferior temporal cortex are more rapid and occur primarily during the task, indicative of motion artifact.