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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) 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.
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pbio.1002272.g006: (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.

Mentions: Although evidence exists for behaviorally relevant modulation of alpha and gamma oscillations in the occipital cortex [13,14], there is evidence that the top-down control signals that produce these modulations originate in the frontal cortex [16,18]. Given that gamma oscillations likely represent a general-purpose mechanism for effective communication [32], we further investigated whether SLF1 asymmetry predicted hemispheric asymmetry of gamma oscillations in prefrontal regions. To do this, we predefined two frontal ROIs: first, the FEF as defined by a meta-analysis of saccade studies [33] and, second, an adjacent region in the superior frontal cortex that has been identified as part of a frontoparietal network underpinning spatial attention and working memory [19,20]. To our surprise, hemispheric gamma modulation asymmetry (delta AMI) was found to correlate strongly with SLF asymmetry in the latter ROI (Fig 6A, r = -0.47, p = 0.017). Notably, the correlations in superior frontal cortex are negative, while they are positive in the occipital cortex. Fig 6B shows statistical maps of the correlation of SLF1 asymmetry with gamma asymmetry for every grid point. Grid points in the frontal cortex show negative correlations, and grid points in the occipital cortex show positive correlations. This means that those subjects with a greater left than right SLF1 volume actually displayed relatively greater gamma modulation in the right than left superior frontal cortex.


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) 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.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4595220&req=5

pbio.1002272.g006: (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.
Mentions: Although evidence exists for behaviorally relevant modulation of alpha and gamma oscillations in the occipital cortex [13,14], there is evidence that the top-down control signals that produce these modulations originate in the frontal cortex [16,18]. Given that gamma oscillations likely represent a general-purpose mechanism for effective communication [32], we further investigated whether SLF1 asymmetry predicted hemispheric asymmetry of gamma oscillations in prefrontal regions. To do this, we predefined two frontal ROIs: first, the FEF as defined by a meta-analysis of saccade studies [33] and, second, an adjacent region in the superior frontal cortex that has been identified as part of a frontoparietal network underpinning spatial attention and working memory [19,20]. To our surprise, hemispheric gamma modulation asymmetry (delta AMI) was found to correlate strongly with SLF asymmetry in the latter ROI (Fig 6A, r = -0.47, p = 0.017). Notably, the correlations in superior frontal cortex are negative, while they are positive in the occipital cortex. Fig 6B shows statistical maps of the correlation of SLF1 asymmetry with gamma asymmetry for every grid point. Grid points in the frontal cortex show negative correlations, and grid points in the occipital cortex show positive correlations. This means that those subjects with a greater left than right SLF1 volume actually displayed relatively greater gamma modulation in the right than left superior frontal cortex.

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.