Hemispheric Asymmetry of Globus Pallidus Relates to Alpha Modulation in Reward-Related Attentional Tasks

Cecilia Mazzetti, Tobias Staudigl, Tom R. Marshall, Johanna M. Zumer, Sean J. Fallon, Ole Jensen

Research output: Contribution to journalArticle

Abstract

Whereas subcortical structures such as the basal ganglia have been widely explored in relation to motor control, recent evidence suggests that their mechanisms extend to the domain of attentional switching. We here investigated the subcortical involvement in reward related top-down control of visual alpha-band oscillations (8-13 Hz), which have been consistently linked to mechanisms supporting the allocation of visuospatial attention. Given that items associated with contextual saliency (e.g., monetary reward or loss) attract attention, it is not surprising that the acquired salience of visual items further modulates. The executive networks controlling such reward-dependent modulations of oscillatory brain activity have yet to be fully elucidated. Although such networks have been explored in terms of corticocortical interactions, subcortical regions are likely to be involved. To uncover this, we combined MRI and MEG data from 17 male and 11 female participants, investigating whether derived measures of subcortical structural asymmetries predict interhemispheric modulation of alpha power during a spatial attention task. We show that volumetric hemispheric lateralization of globus pallidus (GP) and thalamus (Th) explains individual hemispheric biases in the ability to modulate posterior alpha power. Importantly, for the GP, this effect became stronger when the value saliency parings in the task increased. Our findings suggest that the GP and Th in humans are part of a subcortical executive control network, differentially involved in modulating posterior alpha activity in the presence of saliency. Further investigation aimed at uncovering the interaction between subcortical and neocortical attentional networks would provide useful insight in future studies. SIGNIFICANCE STATEMENT Whereas the involvement of subcortical regions into higher level cognitive processing, such as attention and reward attribution, has been already indicated in previous studies, little is known about its relationship with the functional oscillatory underpinnings of said processes. In particular, interhemispheric modulation of alpha band (8-13 Hz) oscillations, as recorded with magnetoencephalography, has been previously shown to vary as a function of salience (i.e., monetary reward/loss) in a spatial attention task. We here provide novel insights into the link between subcortical and cortical control of visual attention. Using the same reward-related spatial attention paradigm, we show that the volumetric lateralization of subcortical structures (specifically globus pallidus and thalamus) explains individual biases in the modulation of visual alpha activity.

Original languageEnglish
Pages (from-to)9221-9236
Number of pages16
JournalJournal of Neuroscience
Volume39
Issue number46
DOIs
Publication statusPublished - 13 Nov 2019

Fingerprint

Globus Pallidus
Reward
Thalamus
Magnetoencephalography
Aptitude
Executive Function
Basal Ganglia
Brain

Bibliographical note

Copyright © 2019 the authors

Keywords

  • attention
  • basal ganglia
  • magnetic resonance imaging
  • magnetoencephalography
  • reward

Cite this

Mazzetti, Cecilia ; Staudigl, Tobias ; Marshall, Tom R. ; Zumer, Johanna M. ; Fallon, Sean J. ; Jensen, Ole. / Hemispheric Asymmetry of Globus Pallidus Relates to Alpha Modulation in Reward-Related Attentional Tasks. In: Journal of Neuroscience. 2019 ; Vol. 39, No. 46. pp. 9221-9236.
@article{2f978289d0e24df9892c6b3df87f8688,
title = "Hemispheric Asymmetry of Globus Pallidus Relates to Alpha Modulation in Reward-Related Attentional Tasks",
abstract = "Whereas subcortical structures such as the basal ganglia have been widely explored in relation to motor control, recent evidence suggests that their mechanisms extend to the domain of attentional switching. We here investigated the subcortical involvement in reward related top-down control of visual alpha-band oscillations (8-13 Hz), which have been consistently linked to mechanisms supporting the allocation of visuospatial attention. Given that items associated with contextual saliency (e.g., monetary reward or loss) attract attention, it is not surprising that the acquired salience of visual items further modulates. The executive networks controlling such reward-dependent modulations of oscillatory brain activity have yet to be fully elucidated. Although such networks have been explored in terms of corticocortical interactions, subcortical regions are likely to be involved. To uncover this, we combined MRI and MEG data from 17 male and 11 female participants, investigating whether derived measures of subcortical structural asymmetries predict interhemispheric modulation of alpha power during a spatial attention task. We show that volumetric hemispheric lateralization of globus pallidus (GP) and thalamus (Th) explains individual hemispheric biases in the ability to modulate posterior alpha power. Importantly, for the GP, this effect became stronger when the value saliency parings in the task increased. Our findings suggest that the GP and Th in humans are part of a subcortical executive control network, differentially involved in modulating posterior alpha activity in the presence of saliency. Further investigation aimed at uncovering the interaction between subcortical and neocortical attentional networks would provide useful insight in future studies. SIGNIFICANCE STATEMENT Whereas the involvement of subcortical regions into higher level cognitive processing, such as attention and reward attribution, has been already indicated in previous studies, little is known about its relationship with the functional oscillatory underpinnings of said processes. In particular, interhemispheric modulation of alpha band (8-13 Hz) oscillations, as recorded with magnetoencephalography, has been previously shown to vary as a function of salience (i.e., monetary reward/loss) in a spatial attention task. We here provide novel insights into the link between subcortical and cortical control of visual attention. Using the same reward-related spatial attention paradigm, we show that the volumetric lateralization of subcortical structures (specifically globus pallidus and thalamus) explains individual biases in the modulation of visual alpha activity.",
keywords = "attention, basal ganglia, magnetic resonance imaging, magnetoencephalography, reward",
author = "Cecilia Mazzetti and Tobias Staudigl and Marshall, {Tom R.} and Zumer, {Johanna M.} and Fallon, {Sean J.} and Ole Jensen",
note = "Copyright {\circledC} 2019 the authors",
year = "2019",
month = "11",
day = "13",
doi = "10.1523/JNEUROSCI.0610-19.2019",
language = "English",
volume = "39",
pages = "9221--9236",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "46",

}

Hemispheric Asymmetry of Globus Pallidus Relates to Alpha Modulation in Reward-Related Attentional Tasks. / Mazzetti, Cecilia; Staudigl, Tobias; Marshall, Tom R.; Zumer, Johanna M.; Fallon, Sean J.; Jensen, Ole.

In: Journal of Neuroscience, Vol. 39, No. 46, 13.11.2019, p. 9221-9236.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Hemispheric Asymmetry of Globus Pallidus Relates to Alpha Modulation in Reward-Related Attentional Tasks

AU - Mazzetti, Cecilia

AU - Staudigl, Tobias

AU - Marshall, Tom R.

AU - Zumer, Johanna M.

AU - Fallon, Sean J.

AU - Jensen, Ole

N1 - Copyright © 2019 the authors

PY - 2019/11/13

Y1 - 2019/11/13

N2 - Whereas subcortical structures such as the basal ganglia have been widely explored in relation to motor control, recent evidence suggests that their mechanisms extend to the domain of attentional switching. We here investigated the subcortical involvement in reward related top-down control of visual alpha-band oscillations (8-13 Hz), which have been consistently linked to mechanisms supporting the allocation of visuospatial attention. Given that items associated with contextual saliency (e.g., monetary reward or loss) attract attention, it is not surprising that the acquired salience of visual items further modulates. The executive networks controlling such reward-dependent modulations of oscillatory brain activity have yet to be fully elucidated. Although such networks have been explored in terms of corticocortical interactions, subcortical regions are likely to be involved. To uncover this, we combined MRI and MEG data from 17 male and 11 female participants, investigating whether derived measures of subcortical structural asymmetries predict interhemispheric modulation of alpha power during a spatial attention task. We show that volumetric hemispheric lateralization of globus pallidus (GP) and thalamus (Th) explains individual hemispheric biases in the ability to modulate posterior alpha power. Importantly, for the GP, this effect became stronger when the value saliency parings in the task increased. Our findings suggest that the GP and Th in humans are part of a subcortical executive control network, differentially involved in modulating posterior alpha activity in the presence of saliency. Further investigation aimed at uncovering the interaction between subcortical and neocortical attentional networks would provide useful insight in future studies. SIGNIFICANCE STATEMENT Whereas the involvement of subcortical regions into higher level cognitive processing, such as attention and reward attribution, has been already indicated in previous studies, little is known about its relationship with the functional oscillatory underpinnings of said processes. In particular, interhemispheric modulation of alpha band (8-13 Hz) oscillations, as recorded with magnetoencephalography, has been previously shown to vary as a function of salience (i.e., monetary reward/loss) in a spatial attention task. We here provide novel insights into the link between subcortical and cortical control of visual attention. Using the same reward-related spatial attention paradigm, we show that the volumetric lateralization of subcortical structures (specifically globus pallidus and thalamus) explains individual biases in the modulation of visual alpha activity.

AB - Whereas subcortical structures such as the basal ganglia have been widely explored in relation to motor control, recent evidence suggests that their mechanisms extend to the domain of attentional switching. We here investigated the subcortical involvement in reward related top-down control of visual alpha-band oscillations (8-13 Hz), which have been consistently linked to mechanisms supporting the allocation of visuospatial attention. Given that items associated with contextual saliency (e.g., monetary reward or loss) attract attention, it is not surprising that the acquired salience of visual items further modulates. The executive networks controlling such reward-dependent modulations of oscillatory brain activity have yet to be fully elucidated. Although such networks have been explored in terms of corticocortical interactions, subcortical regions are likely to be involved. To uncover this, we combined MRI and MEG data from 17 male and 11 female participants, investigating whether derived measures of subcortical structural asymmetries predict interhemispheric modulation of alpha power during a spatial attention task. We show that volumetric hemispheric lateralization of globus pallidus (GP) and thalamus (Th) explains individual hemispheric biases in the ability to modulate posterior alpha power. Importantly, for the GP, this effect became stronger when the value saliency parings in the task increased. Our findings suggest that the GP and Th in humans are part of a subcortical executive control network, differentially involved in modulating posterior alpha activity in the presence of saliency. Further investigation aimed at uncovering the interaction between subcortical and neocortical attentional networks would provide useful insight in future studies. SIGNIFICANCE STATEMENT Whereas the involvement of subcortical regions into higher level cognitive processing, such as attention and reward attribution, has been already indicated in previous studies, little is known about its relationship with the functional oscillatory underpinnings of said processes. In particular, interhemispheric modulation of alpha band (8-13 Hz) oscillations, as recorded with magnetoencephalography, has been previously shown to vary as a function of salience (i.e., monetary reward/loss) in a spatial attention task. We here provide novel insights into the link between subcortical and cortical control of visual attention. Using the same reward-related spatial attention paradigm, we show that the volumetric lateralization of subcortical structures (specifically globus pallidus and thalamus) explains individual biases in the modulation of visual alpha activity.

KW - attention

KW - basal ganglia

KW - magnetic resonance imaging

KW - magnetoencephalography

KW - reward

UR - https://www.jneurosci.org/content/39/46/9221

UR - http://www.scopus.com/inward/record.url?scp=85074964911&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.0610-19.2019

DO - 10.1523/JNEUROSCI.0610-19.2019

M3 - Article

C2 - 31578234

VL - 39

SP - 9221

EP - 9236

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 46

ER -