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

Marshall TR, Bergmann TO, Jensen O - PLoS Biol. (2015)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands.

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.

No MeSH data available.


(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.
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pbio.1002272.g003: (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.

Mentions: Next, we sought to relate individual differences in modulations of the gamma and alpha band activity to properties of the SLF. Spherical deconvolution tractography [25,28] was used to reconstruct the SLF branches from the diffusion data. Consistent with previous research [21,23], a network of three branches in each hemisphere was reconstructed (Fig 3A). For each of the three SLF branches, a hemispheric asymmetry index was computed (100% (volume_left–volume_right)/ (volume_left + volume_right); see Materials and Methods), quantifying whether each subject had greater tract volume in the left or right hemisphere. Nonoverlapping regions were identified as regions of interest (ROIs) in prefrontal cortex and then used for seeding the fiber tracking. This ensured that the fiber bundles were well separated. The medial SLF1 branches were defined as fibers passing through superior frontal gyrus, SLF2 as passing through middle frontal gyrus, and SLF3 as passing through precentral gyrus (see Materials and Methods). Replicating previous findings [21], the SLF3 was right-lateralized at the group level, whereas SLF1 and SLF2 did not show evidence of lateralization at the group level (see Fig 3B). Furthermore, a modulation asymmetry index was also calculated for each subject’s MEG data indicating whether—for both alpha and gamma oscillations—that subject displayed a stronger degree of power modulation with attention in the left or right hemisphere (ΔAMI = (- AMIleft,j)—AMIright,j; see Materials and Methods). We derived the alpha and gamma modulation values (ΔAMI) from the anatomical regions demonstrating strongest attentional modulation for each band, namely the superior occipital cortex for the alpha band and the middle occipital cortex for the gamma band (see Fig 2). Alpha and gamma asymmetry were not correlated with each other (r = -0.148, p = 0.47). We then correlated alpha and gamma asymmetry with the volumetric asymmetry of the three SLF branches.


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

Marshall TR, Bergmann TO, Jensen O - PLoS Biol. (2015)

(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.
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pbio.1002272.g003: (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.
Mentions: Next, we sought to relate individual differences in modulations of the gamma and alpha band activity to properties of the SLF. Spherical deconvolution tractography [25,28] was used to reconstruct the SLF branches from the diffusion data. Consistent with previous research [21,23], a network of three branches in each hemisphere was reconstructed (Fig 3A). For each of the three SLF branches, a hemispheric asymmetry index was computed (100% (volume_left–volume_right)/ (volume_left + volume_right); see Materials and Methods), quantifying whether each subject had greater tract volume in the left or right hemisphere. Nonoverlapping regions were identified as regions of interest (ROIs) in prefrontal cortex and then used for seeding the fiber tracking. This ensured that the fiber bundles were well separated. The medial SLF1 branches were defined as fibers passing through superior frontal gyrus, SLF2 as passing through middle frontal gyrus, and SLF3 as passing through precentral gyrus (see Materials and Methods). Replicating previous findings [21], the SLF3 was right-lateralized at the group level, whereas SLF1 and SLF2 did not show evidence of lateralization at the group level (see Fig 3B). Furthermore, a modulation asymmetry index was also calculated for each subject’s MEG data indicating whether—for both alpha and gamma oscillations—that subject displayed a stronger degree of power modulation with attention in the left or right hemisphere (ΔAMI = (- AMIleft,j)—AMIright,j; see Materials and Methods). We derived the alpha and gamma modulation values (ΔAMI) from the anatomical regions demonstrating strongest attentional modulation for each band, namely the superior occipital cortex for the alpha band and the middle occipital cortex for the gamma band (see Fig 2). Alpha and gamma asymmetry were not correlated with each other (r = -0.148, p = 0.47). We then correlated alpha and gamma asymmetry with the volumetric asymmetry of the three SLF branches.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands.

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.

No MeSH data available.