Frontoparietal Structural Connectivity Mediates the Top-Down Control of Neuronal Synchronization Associated with Selective Attention

Abstract

Neuronal synchronization reflected by oscillatory brain activity has been strongly implicated in the mechanisms supporting selective gating. We here aimed at identifying the anatomical pathways in humans supporting the top-down control of neuronal synchronization. We first collected diffusion imaging data using magnetic resonance imaging to identify the medial branch of the superior longitudinal fasciculus (SLF), a white-matter tract connecting frontal control areas to parietal regions. We then quantified the modulations in oscillatory activity using magnetoencephalography in the same subjects performing a spatial attention task. We found that subjects with a stronger SLF volume in the right compared to the left hemisphere (or vice versa) also were the subjects who had a better ability to modulate right compared to left hemisphere alpha and gamma band synchronization, with the latter also predicting biases in reaction time. Our findings implicate the medial branch of the SLF in mediating top-down control of neuronal synchronization in sensory regions that support selective attention.

Fig 1. (A) Experimental paradigm. Each trial began with one of four visual cues, instructing the subject either to attend to the left luminance pedestal, the right luminance pedestal, to both luminance pedestals, or to passively fixate. After a 1.5 s fixed interval, a pair of Gabor patches appeared in both luminance pedestals. One Gabor patch was always diagonally oriented (45° clockwise or counterclockwise from vertical), and the other cardinally oriented (horizontal or vertical). In the "attend left" and "attend right" conditions, the diagonal patch appeared respectively in the left or right pedestal; in the "attend both" and "attend neither" conditions, location of the diagonal patch was random. Subjects had to discriminate the orientation of the diagonal patch. (B) Analysis of behavioral data revealed that spatial cueing significantly improved both reaction time and accuracy, whereas target hemifield did not alter reaction time or accuracy.

Fig 2. Time-frequency analysis and source reconstructions of attentional modulation of anticipatory alpha and stimulus-induced gamma oscillations.

(A,B) For left and right occipital MEG sensors. “Attention left” trials were compared to “attention right” trials. Bilateral attentional modulation is clearly visible in the alpha band during the cue-target interval, and bilateral modulation of stimulus-induced gamma oscillations is clearly visible during the post-stimulus interval. (C) Grand average alpha modulation index (attention left versus attention right) calculated for cue-target interval (350–1,350 ms post-cue); alpha modulation is strongest in the bilateral superior occipital cortex. (D) Grand average gamma modulation index calculated for post-stimulus interval (1,700–2,100 ms post-cue); gamma modulation is strongest in the bilateral middle occipital cortex.

Fig 3. (A) Tractographic rendering of SLF branches in one subject obtained using diffusion MRI. The medial branch (SLF1) is shown in sky blue, the middle branch (SLF2) is shown in dark blue, and the lateral branch (SLF3) is shown in purple. These branches were identified by following the tracts intersecting coronal slices passing through both parietal cortex and, respectively, the superior frontal gyrus (SLF1), middle frontal gyrus (SLF2), and precentral gyrus (SLF3). (B) Group average hemispheric tract asymmetry for the three SLF branches. Consistent with previous work [21], only SLF3 shows consistent right lateralization (t(25) = -6.02, p < 0.0001). SLF1 and SLF2 are not lateralized (SLF1: t(25) = 0.17, p = 0.87. SLF2: t(25) = -0.51, p = 0.62). Error bars represent 95% confidence intervals. *** indicates p < 0.0001.

Fig 4. (A) Correlation of gamma modulation asymmetry in the middle occipital cortex (see Fig 2) with volumetric asymmetry of the three SLF branches. The gamma modulation asymmetry was calculated by comparing the degree of attentional modulation (left versus right spatial cue) in the right versus the left hemisphere. In the case of the SLF1, gamma modulation asymmetry was strongly positively correlated with volumetric hemispheric asymmetry (p = 0.0016, significant at the p < 0.005 level after Bonferroni correction for three comparisons). Neither SLF2 nor SLF3 showed such a correlation. (B) The same correlations but for alpha modulation asymmetry in superior occipital cortex (see Fig 2). Only SLF1 volumetric hemispheric asymmetry showed a significant negative correlation with alpha modulation asymmetry (p = 0.0096, significant at the p < 0.05 level after Bonferroni correction for three comparisons). As such, subjects with stronger left than right tracks in SLF1 were able to modulate the left compared to right hemisphere alpha and gamma power to a larger degree.

Fig 5. Correlation of oscillatory hemispheric asymmetry with behavioral measures.

(A) Correlation of gamma asymmetry with reaction time benefit from left versus right spatial cues. Subjects benefitted relatively more from (i.e., responded faster to) a spatial cue contralateral to the hemisphere in which they showed greater gamma modulation. This supports the notion that gamma leads to enhanced stimulus processing. (B) As A, but for alpha asymmetry. Here no relationship was observed. (C) Accuracy benefit from left versus right spatial cues. No relationship was observed between accuracy benefit and gamma asymmetry. (D) As C, but for alpha asymmetry. Again, no relationship was observed.

Fig 6. (A) Correlation of SLF1 asymmetry with gamma-band hemispheric asymmetry in superior frontal cortex (−26 +6 +56; as defined in [19]). A clear negative correlation is observed, which—notably—is opposite in sign to the correlation between SLF1 asymmetry and occipital gamma modulation asymmetry. (B) Topographic map of correlation of gamma-band hemispheric asymmetry with SLF1 asymmetry. Map is thresholded at p < 0.05, uncorrected. MNI coordinates for slices: +66, +54. A sign reversal is evident for the frontal grid points compared to the posterior grid points. Whereas stronger gamma modulation in the occipital cortex is associated with a relatively larger ipsilateral SLF1, in the frontal cortex it is associated with a relatively larger contralateral SLF1.