Specialized neural dynamics for verbal and tonal memory: fMRI evidence in congenital amusia

Abstract

Behavioral and neuropsychological studies have suggested that tonal and verbal short-term memory are supported by specialized neural networks. To date however, neuroimaging investigations have failed to confirm this hypothesis. In this study, we investigated the hypothesis of distinct neural resources for tonal and verbal memory by comparing typical nonmusician listeners to individuals with congenital amusia, who exhibit pitch memory impairments with preserved verbal memory. During fMRI, amusics and matched controls performed delayed-match-to-sample tasks with tones and words and perceptual control tasks with the same stimuli. For tonal maintenance, amusics showed decreased activity in the right auditory cortex, inferior frontal gyrus (IFG) and dorso-lateral-prefrontal cortex (DLPFC). Moreover, they exhibited reduced right-lateralized functional connectivity between the auditory cortex and the IFG during tonal encoding and between the IFG and the DLPFC during tonal maintenance. In contrasts, amusics showed no difference compared with the controls for verbal memory, with activation in the left IFG and left fronto-temporal connectivity. Critically, we observed a group-by-material interaction in right fronto-temporal regions: while amusics recruited these regions less strongly for tonal memory than verbal memory, control participants showed the reversed pattern (tonal > verbal). By benefitting from the rare condition of amusia, our findings suggest specialized cortical systems for tonal and verbal short-term memory in the human brain.

Keywords: auditory; brain networks; inferior frontal gyrus; memory; tone deafness.

Figure 1

(a) Examples of the stimuli used in the memory and perception tasks. (b) Performance of amusic and control groups (white, controls; red, amusics) in terms of d′, presented as a function of material (orange, tonal; blue, verbal) and task (M: memory task; P: perception task). Error bars indicate SEM. (c) Design for the fMRI experiment, the sparse sampling protocol, timeline of events during one trial, and brain activity for all participants. Left panel: For maintenance runs, the volume acquisition occurred just before the second sequence (at the end of the silent delay), the acquisition thus starting from 5,500 to 6,000 ms after the end of S1. Sections show brain regions where activation was increased during maintenance in memory trials (tonal top panel and verbal lower panel) as compared with baseline (silence) in all participants. FDR corrected p < .05. The comparison between perception trials and baseline did not show any significant cluster. These scans were performed for both tonal and verbal trials. Right panel: For encoding runs (two runs, tonal material only), acquisition started 3,500–4,000 ms after the end of the S1 sequence. Sections show brain regions where activity was increased during encoding in memory trials (tonal material) as compared with baseline (silence) and perception trials vs. baseline (silence) in all participants. FDR corrected p < .05. Results are displayed on the single subject T1 image in the MNI space provided by SPM12 [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Functional imaging results. (a) Maintenance scans for verbal material (blue squares). Top panel: Memory versus perception for all participants FDR‐corrected p < .05. Scatter plot represents parameter estimates (p.e.) extracted from the left IFG for each group (red: amusics, white: controls) as a function of behavioral performance in the memory task for words; bottom panel: Seed‐to‐voxel functional connectivity results for the contrast memory vs. perception (verbal), all participants. Black dot indicates the seed region in the left anterior STG. (b) Maintenance scans for tonal material (orange squares). Left panel: Controls versus amusics (memory vs. perception) FDR‐corrected p < .05. Scatter plot represents parameter estimates (p.e.) extracted from the right IFG for the control group (white circles) as a function of their behavioral performance in the memory task for tones. Right top panel: Amusics versus controls (memory vs. perception). Scatter plot represents parameter estimates (p.e.) extracted from the left STG for the amusic group (red circles) as a function of their behavioral performance in the memory task for tones. Right lower panel: Seed‐to‐voxel functional connectivity results for the contrast controls versus amusics (memory vs. perception tonal). Black dot indicates the seed region in the right IFG. All results are displayed on the single subject T1 in the MNI space provided by SPM12. The areas of activation are detailed in Supporting Information Table S2 [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Functional imaging results, maintenance scans. (a) Group by material interaction, p < .05 FDR‐corrected. Memory vs. perception contrasts were performed at the first level each material for all participants. (b) Bar plots represent parameter estimates for the difference tonal minus verbal for significant regions for each group (red, amusics; white, controls). Errors bars represent the SEM [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Functional imaging results, encoding scans for tonal material. (a) Memory versus perception for all participants FDR‐corrected p < .05. Results are displayed single subject T1 in the MNI space provided by SPM12. The areas of activation are detailed in Supporting Information Table S2. Errors bars represent the SEM. (b) Seed to voxel functional connectivity results for the contrast controls > amusics (memory vs. perception tonal). Black dot indicates the seed region in the right anterior STG [Color figure can be viewed at http://wileyonlinelibrary.com]