The right inferior frontal gyrus processes nested non-local dependencies in music

Abstract

Complex auditory sequences known as music have often been described as hierarchically structured. This permits the existence of non-local dependencies, which relate elements of a sequence beyond their temporal sequential order. Previous studies in music have reported differential activity in the inferior frontal gyrus (IFG) when comparing regular and irregular chord-transitions based on theories in Western tonal harmony. However, it is unclear if the observed activity reflects the interpretation of hierarchical structure as the effects are confounded by local irregularity. Using functional magnetic resonance imaging (fMRI), we found that violations to non-local dependencies in nested sequences of three-tone musical motifs in musicians elicited increased activity in the right IFG. This is in contrast to similar studies in language which typically report the left IFG in processing grammatical syntax. Effects of increasing auditory working demands are moreover reflected by distributed activity in frontal and parietal regions. Our study therefore demonstrates the role of the right IFG in processing non-local dependencies in music, and suggests that hierarchical processing in different cognitive domains relies on similar mechanisms that are subserved by domain-selective neuronal subpopulations.

Figure 1

(A) Example stimuli. Auditory musical sequences were formed by concatenating three-tone motifs according to the nested atonal grammar A_nA_n−1…A₁B₁…B_n−1B_n. Each motif belonged to one of two states (A,B), and one of four categories (see lower right, and also Table 1). Categories of A-motifs were randomly concatenated without replacement and were matched by the B-motifs in reverse order. The sequences were manipulated along two factors: GRAMMATICALITY (grammatical vs. ungrammatical) and LEVEL OF EMBEDDING (ONE-LoE (n = 2) vs. TWO-LoE (n = 3)). Ungrammatical sequences contained exactly one violated B-motif for which its state or category (but not both) was interchanged. Audio versions of the exemplar sequences can be found as Supplementary Audio clips SA1–6. (B) Experimental paradigm. Musicians discriminated the grammaticality of 144 novel nested atonal musical sequences, equally divided between combinations of the factors GRAMMATICALITY (grammatical vs. ungrammatical) and LEVEL OF EMBEDDING (ONE-LoE vs. TWO-LoE), during fMRI scanning. Each trial began with a fixation cross at the centre of the screen, and an auditory sequence was presented after a jitter. The symbols ‘Y’ and ‘N’ then respectively appeared to the lower left and right of the fixation cross (pseudo-randomised across trials) and participants were given a 4s-time window to judge the grammatically of the presented sequence. Feedback was then given and a new trial ensued. The nested grammar was previously acquired in a behavioural session around 3.5 weeks before the fMRI experiment.

Figure 2

Behavioural results. Sensitivity in discriminating the grammaticality of nested musical sequences was significantly higher for ONE compared to TWO levels of embedding. Error-bars indicate standard error. *Indicates p < 0.05.

Figure 3

(A) Whole-brain activations for main effects of grammaticality and level of embedding (LoE) on discriminating the grammaticality of nested musical sequences. The contrast UNGRAMMATICAL > GRAMAMTICAL yielded significant clusters (red) in the right inferior frontal gyrus, right middle frontal gyrus, bilateral anterior insular cortices, the pre-supplementary motor area, and the right posterior middle temporal gyrus. Contrasting sequences with TWO-LoE > ONE-LoE yielded significant clusters (blue) bilaterally in the middle frontal gyrus and inferior parietal lobule. Reported clusters were corrected for multiple comparisons voxel-wise at a threshold of p < 0.05 and an extent of 4 voxels. (B) PPI analysis on significant clusters of the refined model where ungrammatical sequences only included non-local category violations. Using the refined model, activity was observed in the right pars opercularis, right pars triangularis, and bilateral anterior insular cortices for the contrast UNGRAMMATICAL > GRAMAMTICAL (seed regions in red), and the right middle frontal gyrus and right inferior parietal lobule for the contrast TWO-LoE > ONE-LoE (seed regions in blue). Dotted lines indicate significantly-increased functional connectivity between seed regions of significant clusters in the experimental context of UNGRAMMATICAL sequences compared to GRAMMATICAL. Results were corrected for multiple comparisons voxel-wise at a threshold of p < 0.05 and an extent of 4 voxels. (C) Positive correlation between sensitivity in discriminating the grammaticality of nested musical sequences and increase in task modulated functional connectivity (r = 0.55, p = 0.03, 1-tailed test; corrected). Shaded region is the 95% confidence band of the linear regression line.