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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.


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.
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pbio.1002272.g005: 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.

Mentions: Having demonstrated a link between hemispheric asymmetry of SLF1 and both anticipatory alpha and stimulus-induced gamma band modulations in visual cortex, we further tested if these effects were predictive of subjects’ task performance. Accordingly, we quantified the degree to which subjects benefitted (in terms of reaction time and accuracy) from a left versus a right cue in comparison to the control condition with no spatial cue (see Materials and Methods). This hemifield specific asymmetry of the cueing benefit correlated with the hemispheric asymmetry of occipital gamma power modulation (ΔAMI; Fig 5A, r = -0.40, p < 0.05) but did not correlate with alpha power modulation (Fig 5B, r = 0.03, p = 0.89). The negative correlation value means that subjects with relatively stronger gamma modulation in the left occipital cortex than in the right occipital cortex benefitted more from a right cue than a left cue. This is fully commensurate with the notion that visual cortical gamma modulation in the hemisphere contralateral to target presentation boosts effective synaptic gain and thus enhances stimulus processing. No correlation was observed between accuracy benefit and hemispheric asymmetry of occipital gamma modulation (Fig 5C, r = 0.16, p = 0.45) or alpha modulation (Fig 5D, r = 0.31 p = 0.12).


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

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

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.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4595220&req=5

pbio.1002272.g005: 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.
Mentions: Having demonstrated a link between hemispheric asymmetry of SLF1 and both anticipatory alpha and stimulus-induced gamma band modulations in visual cortex, we further tested if these effects were predictive of subjects’ task performance. Accordingly, we quantified the degree to which subjects benefitted (in terms of reaction time and accuracy) from a left versus a right cue in comparison to the control condition with no spatial cue (see Materials and Methods). This hemifield specific asymmetry of the cueing benefit correlated with the hemispheric asymmetry of occipital gamma power modulation (ΔAMI; Fig 5A, r = -0.40, p < 0.05) but did not correlate with alpha power modulation (Fig 5B, r = 0.03, p = 0.89). The negative correlation value means that subjects with relatively stronger gamma modulation in the left occipital cortex than in the right occipital cortex benefitted more from a right cue than a left cue. This is fully commensurate with the notion that visual cortical gamma modulation in the hemisphere contralateral to target presentation boosts effective synaptic gain and thus enhances stimulus processing. No correlation was observed between accuracy benefit and hemispheric asymmetry of occipital gamma modulation (Fig 5C, r = 0.16, p = 0.45) or alpha modulation (Fig 5D, r = 0.31 p = 0.12).

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.