Inter-subject synchronization of brain responses during natural music listening

Abstract

Music is a cultural universal and a rich part of the human experience. However, little is known about common brain systems that support the processing and integration of extended, naturalistic 'real-world' music stimuli. We examined this question by presenting extended excerpts of symphonic music, and two pseudomusical stimuli in which the temporal and spectral structure of the Natural Music condition were disrupted, to non-musician participants undergoing functional brain imaging and analysing synchronized spatiotemporal activity patterns between listeners. We found that music synchronizes brain responses across listeners in bilateral auditory midbrain and thalamus, primary auditory and auditory association cortex, right-lateralized structures in frontal and parietal cortex, and motor planning regions of the brain. These effects were greater for natural music compared to the pseudo-musical control conditions. Remarkably, inter-subject synchronization in the inferior colliculus and medial geniculate nucleus was also greater for the natural music condition, indicating that synchronization at these early stages of auditory processing is not simply driven by spectro-temporal features of the stimulus. Increased synchronization during music listening was also evident in a right-hemisphere fronto-parietal attention network and bilateral cortical regions involved in motor planning. While these brain structures have previously been implicated in various aspects of musical processing, our results are the first to show that these regions track structural elements of a musical stimulus over extended time periods lasting minutes. Our results show that a hierarchical distributed network is synchronized between individuals during the processing of extended musical sequences, and provide new insight into the temporal integration of complex and biologically salient auditory sequences.

Fig. 1

Stimuli. Spectrograms of the Natural Music (left), Spectrally-Rotated (center) and Phase- Scrambled (right) conditions. The first of the four symphonies played during the fMRI scan is plotted for all conditions. Spectral-rotation and phase-scrambling was performed on each of the four symphonies comprising the stimulus set for the fMRI experiment.

Fig. 2

Inter-subject synchronization in subcortical auditory structures. (A) Axial slices (Z = −11) reveal ISS in the inferior colliculus (IC) of the midbrain in response to the Natural Music (left) but not to the Spectrally-Rotated (center) and Phase-Scrambled music (right) conditions. Images were thresholded using a voxel-wise statistical height threshold of (P < 0.005), with corrections for multiple comparisons at the cluster level (P < 0.05; 50 voxels). (B) Results show suprathreshold voxels throughout the IC (top) and MGN (bottom) for the Natural Music > Spectrally-Rotated (left) and Natural Music > Phase-Scrambled (right) comparisons. Sub-cortical ROIs were thresholded using a voxel-wise statistical height threshold of (P < 0.05), uncorrected. Functional images are superimposed on a standard brain from a single normal subject (MNI_152_T1_1mm_brain.nii; MRIcroN (Rorden & Brett, 2000)).

Fig. 3

Inter-subject synchronization in auditory cortex. Axial slices showing ISS for the Natural Music (left), Spectrally-Rotated (center) and Phase-Scrambled (right) conditions in dorsal (Z = 8; top) and ventral (Z = −6; bottom) views of auditory cortex. Results indicate ISS throughout auditory cortex, including Heschl’s gyrus (HG, blue), planum temporale (PT, cyan), posterior superior temporal gyrus (pSTG, pink), and planum polare (PP, green), for the Natural Music and Spectrally-Rotated conditions but not for the Phase-Scrambled condition. Images were thresholded using a voxel-wise statistical height threshold of (P < 0.005), with corrections for multiple comparisons at the cluster level (P < 0.05; 50 voxels).

Fig. 4

ISS Difference maps in auditory cortex. Images show ISS difference maps for Natural Music > Spectrally-Rotated (left) and Natural Music > Phase-scrambled (right) comparisons. Results show no significant differences across auditory cortex for the Natural Music > Spectrally-Rotated comparison, but many suprathreshold voxels across these regions for the Natural Music > Phase-Scrambled comparison. Difference maps were thresholded using a voxel-wise statistical height threshold of (P < 0.005), with corrections for multiple comparisons at the cluster level (P < 0.05; 50 voxels).

Fig. 5

Inter-subject synchronization in fronto-parietal cortex. Coronal slices showing ISS for the Natural Music (left), Spectrally-Rotated (center) and Phase-Scrambled (right) conditions in anterior (Y = 20; top) and posterior (Y = −50; bottom) views of the brain. Results indicate ISS for Natural Music in right hemisphere IFG, including BA 45 and 47, and parietal cortex, including the PGa subregion of the angular gyrus and the superior parietal lobule (SPL). ISS was greatly reduced across these frontal and parietal regions for both the Spectrally-Rotated and Phase-Scrambled control conditions. Images were thresholded using a voxel-wise statistical height threshold of (P < 0.005), with corrections for multiple comparisons at the cluster level (P < 0.05; 50 voxels).

Fig. 6

ISS difference maps in fronto-parietal cortex. Images show ISS difference maps in frontal and parietal cortex for Natural Music > Spectrally-Rotated (left) and Natural Music > Phase-Scrambled (right) comparisons. Results show significant differences in BAs 45 and 47 of IFG (top), as well as PGa and IPS of parietal cortex (bottom), for both stimulus comparisons. Images were thresholded using a voxel-wise statistical height threshold of (P < 0.005), with corrections for multiple comparisons at the cluster level (P < 0.05; 50 voxels).

Fig. 7

Inter-subject synchronization in motor-planning cortical regions. (A) Coronal (Y = −7) and sagittal (X = 13) slices shows ISS throughout the pre-motor cortex (PMC) and mid-cingulate cortex (MCC), respectively, in response to the Natural Music (left) condition. ISS was less prevalent in the both of these motor-planning regions for the Spectrally-Rotated (center) and Phase-Scrambled (right) condition. (B) Results show suprathreshold voxels in the right PMC and MCC for the Natural Music > Spectrally-Rotated and Natural Music > Phase-Scrambled comparisons. Images were thresholded using a voxel-wise statistical height threshold of (P < 0.005), with corrections for multiple comparisons at the cluster level (P < 0.05; 50 voxels).

Fig. 8

Inter-subject spectral coherence analysis in three brain regions. Representative examples of five pairs of subject-to-subject cross-spectra during the Natural Music condition in the IC (top row), HG (middle row), and IFG (bottom row). Intermittent and isolated periods of spectral coherence over time were observed, indicating that ISS does not arise from spectro-temporally invariant neural responses and stimulus-following. Sub1 = Subject 1, Sub2 = Subject 2.