Functional architecture of verbal and tonal working memory: an FMRI study

Abstract

This study investigates the functional architecture of working memory (WM) for verbal and tonal information during rehearsal and articulatory suppression. Participants were presented with strings of four sung syllables with the task to remember either the pitches (tonal information) or the syllables (verbal information). Rehearsal of verbal, as well as of tonal information activated a network comprising ventrolateral premotor cortex (encroaching Broca's area), dorsal premotor cortex, the planum temporale, inferior parietal lobe, the anterior insula, subcortical structures (basal ganglia and thalamus), as well as the cerebellum. The topography of activations was virtually identical for the rehearsal of syllables and pitches, showing a remarkable overlap of the WM components for the rehearsal of verbal and tonal information. When the WM task was performed under articulatory suppression, activations in those areas decreased, while additional activations arose in anterior prefrontal areas. These prefrontal areas might contain additional storage components of verbal and tonal WM that are activated when auditory information cannot be rehearsed. As in the rehearsal conditions, the topography of activations under articulatory suppression was nearly identical for the verbal as compared to the tonal task. Results indicate that both the rehearsal of verbal and tonal information, as well as storage of verbal and tonal information relies on strongly overlapping neuronal networks. These networks appear to partly consist of sensorimotor-related circuits which provide resources for the representation and maintenance of information, and which are remarkably similar for the production of speech and song.

Figure 1

Experimental design. The six example trials illustrate the six different experimental conditions, each trial had a duration of 13 s and began with a visual cue (V R = verbal (syllable) rehearsal, V S = verbal (syllable) suppression, T R = tonal (pitch) rehearsal, T S = tonal (pitch) suppression, N 0 = not memorize anything without rehearsing or singing a song, N S = not memorize anything and sing the song). The cue was followed by the presentation of the stimulus sequence. In the subsequent rehearsal conditions, subjects covertly rehearsed either the syllables (V R) or the pitches (T R). During the suppression conditions (V S, T S), subjects covertly sang a children's song while trying to maintain either the verbal (V S) or the tonal information (T S) in their memory. Then, a probe sequence was presented, followed by a silence period of 2.35 s during which participants had to indicate whether the probe sequence was identical to the initial sequence (verbal and tonal conditions). In the control conditions (N 0, N S), in which participants did not have to memorize the initial sequence, participants had to indicate whether each of the syllables was played forward (forward speech) or backward (backward speech).

Figure 2

Behavioral data of verbal and tonal WM during rehearsal (shaded bars), and of verbal and tonal WM under simultaneous articulatory suppression (nonshaded bars). Participants performed better in the verbal than in the tonal conditions. Note the significant drop in performance (compared to the rehearsal conditions) during maintenance of both verbal and tonal information under articulatory suppression.

Figure 3

Activations during verbal (A) and tonal (B) rehearsal (contrasted to the control condition in which subjects did neither sing nor memorize; P < 0.05 corrected for multiple comparisons). Both tasks activated a network comprising the ventrolateral premotor cortex (vlPMC), the dorsal precentral gyrus, the intraparietal sulcus (IPS) extending into the supramarginal gyrus (SMG), and the planum temporale (p.t.). In the left hemisphere, the pars triangularis of the IFG was activated only during the tonal rehearsal. (C) Shows areas that were significantly activated during both verbal and tonal rehearsal. (D) Illustration of individually adjusted ROIs (for the verbal rehearsal condition). In each cluster, each circle represents the ROI coordinate of one participant.

Figure 4

Activations during maintenance of verbal (A) and maintenance of tonal (B) information under articulatory suppression (contrasted to the control condition in which subjects covertly sung, but did not memorize; P < 0.05 corrected for multiple comparisons). During both verbal and tonal conditions, activations were observed in the vlPMC (extending into the pars opercularis/Broca's area), the anterior insula, the right cerebellum, and the right ventral striatum (not shown). Additional activations were indicated in the pars triangularis, and in the inferior frontal sulcus. The inset in (B) shows that the latter activation extended anteriorly along the upper bank of the IFS into the frontomarginal/intermediate frontal sulcus (P < 0.05 uncorrected). (C) Shows areas that were significantly activated during both conditions.

Figure 5

Activations elicited during covert singing (contrasted to the control condition in which subjects did not sing; P < 0.05 corrected for multiple comparisons).