Elsevier

NeuroImage

Volume 165, 15 January 2018, Pages 222-237
NeuroImage

High-alpha band synchronization across frontal, parietal and visual cortex mediates behavioral and neuronal effects of visuospatial attention

https://doi.org/10.1016/j.neuroimage.2017.10.044Get rights and content

Highlights

  • Large-scale high-alpha band synchrony characterizes visuospatial attention.

  • High-alpha band phase synchrony connects frontal, parietal and visual cortices.

  • Phase synchrony strength co-varies with visual cortex low-alpha amplitude suppression.

  • Phase synchrony strength co-varies with attentional modulations of reaction times.

  • High-alpha synchrony may support attentional top-down coordination.

Abstract

Visuospatial attention prioritizes processing of attended visual stimuli. It is characterized by lateralized alpha-band (8–14 Hz) amplitude suppression in visual cortex and increased neuronal activity in a network of frontal and parietal areas. It has remained unknown what mechanisms coordinate neuronal processing among frontoparietal network and visual cortices and implement the attention-related modulations of alpha-band amplitudes and behavior. We investigated whether large-scale network synchronization could be such a mechanism. We recorded human cortical activity with magnetoencephalography (MEG) during a visuospatial attention task. We then identified the frequencies and anatomical networks of inter-areal phase synchronization from source localized MEG data. We found that visuospatial attention is associated with robust and sustained long-range synchronization of cortical oscillations exclusively in the high-alpha (10–14 Hz) frequency band. This synchronization connected frontal, parietal and visual regions and was observed concurrently with amplitude suppression of low-alpha (6–9 Hz) band oscillations in visual cortex. Furthermore, stronger high-alpha phase synchronization was associated with decreased reaction times to attended stimuli and larger suppression of alpha-band amplitudes. These results thus show that high-alpha band phase synchronization is functionally significant and could coordinate the neuronal communication underlying the implementation of visuospatial attention.

Introduction

Attention reconciles the brain's limited processing capacity with the unlimited flow of sensory input by selecting behaviorally relevant stimuli from irrelevant sensory information. Anticipatory endogenous visuospatial attention improves psychophysical performance in the attended location of the visual field in the absence of eye movement (Posner, 1980) by enhancing neuronal processing of attended stimuli compared to the processing of unattended stimuli in respective sensory cortices (Corbetta and Shulman, 2002, Kastner and Ungerleider, 2000). In electro- (EEG) and magnetoencephalography (MEG) data, anticipatory visuospatial attention suppresses local alpha-band amplitudes more in the visual cortex contralateral to than ipsilateral to the attended hemifield (Capilla et al., 2014, Gould et al., 2011, van Dijk et al., 2008). As alpha suppression is correlated with behavioral performance in both visual and somatosensory tasks with larger suppression being associated with better performance (Iemi et al., 2017, Thut et al., 2006, van Dijk et al., 2008), it is thought to be mechanistically linked to anticipatory attention, possibly through associated changes in neuronal excitability or gain modulations (Iemi et al., 2017, Lange et al., 2013). Local alpha oscillations are thus thought to underlie the inhibition of behaviorally relevant attended information (Jensen and Mazaheri, 2010, Klimesch et al., 2007). Yet, the mechanisms that coordinate the alpha amplitude suppression in sensory cortical areas have remained unknown.

Attentional functions are carried out by the intraparietal sulcus (IPS), superior parietal lobule (SPL), and frontal eye fields (FEF) which together form the dorsal attention network (DAN) (Corbetta and Shulman, 2002, Kastner and Ungerleider, 2000, Petersen and Posner, 2012). The key hubs of this network exhibit mutually correlated blood-oxygenation-level dependent (BOLD) signals (Spadone et al., 2015, Szczepanski et al., 2013). Furthermore, BOLD signal in DAN is biased by visuospatial attention (Szczepanski et al., 2010) and co-varies with attention-related modulations of alpha-band amplitudes in visual cortex (Liu et al., 2016). Finally, the perturbation of neuronal activity in key hubs of DAN with transcranial magnetic stimulation (TMS) modulates the effects of attention on both behavior and alpha-band suppression in visual cortex (Capotosto et al., 2009, Capotosto et al., 2015). DAN is therefore thought to be the brain network responsible for implementing anticipatory visuospatial attention but how neuronal communication is coordinated in DAN and between DAN and the visual system has remained poorly understood.

Neuronal synchronization in the beta (14–30 Hz) and gamma (30–120 Hz) bands has been proposed to coordinate attention-related neuronal processing at sub-second time-scales (Fries, 2015, Miller and Buschman, 2013, Tallon-Baudry, 2012, Womelsdorf and Everling, 2015, Womelsdorf and Fries, 2007). While local field potential (LFP) recordings in non-human primates support this hypothesis (Buschman and Miller, 2007, Gregoriou et al., 2009, Womelsdorf et al., 2007), such strong evidence is lacking for humans. Signal mixing and source leakage hinder reliable estimation of inter-areal synchronization in MEG/EEG sensor-level and source-level analyses respectively (Palva and Palva, 2012, Schoffelen and Gross, 2009). Consequently, only a few prior studies have addressed the role of long-range phase synchronization in attention. Anticipatory visuospatial attention is associated with the lateralization of long-range coherence in the gamma-band between FEF and visual cortex and in the alpha-band between parietal and visual cortex in MEG data (Siegel et al., 2008). Lateralization of alpha-band synchronization between posterior parietal (PPC) and visual cortex during visuospatial attention was also observed in source-reconstructed EEG data (Doesburg et al., 2009). However, as these studies only addressed the differences in synchronization between contra- and ipsilateral hemispheres and were limited to examining small sets of regions-of-interest (ROIs), the complete networks of cortical phase coupling putatively underlying visuospatial attention have remained unidentified and under debate (Palva and Palva, 2007, Palva and Palva, 2011, Sadaghiani and Kleinschmidt, 2016).

We propose here that long-range alpha-band phase synchronization coordinates neuronal processing across relevant cortical areas to support visuospatial attention. We first hypothesized that phase synchronization should be strengthened in task-relevant networks encompassing frontal, parietal and visual cortices during anticipatory visuospatial attention. We further hypothesized that if such synchronization is functionally significant, it should predict attention-related modulations of alpha-amplitude and behavioral performance. To test these hypotheses, we recorded MEG data during a Posner-like cued visuospatial discrimination task. We quantified large-scale network synchronization associated with visuospatial attention using advanced data-analysis techniques and source-localization of the MEG data. To avoid the confounds inherent to frequency- and ROI-limited analyses, we made no a priori selection of frequency-bands- or cortical-sources-of-interest. We then identified the most central connections and key cortical areas of significantly strengthened phase synchronized networks using graph theory and investigated their lateralization patterns. Finally, to assess the functional significance of phase synchronization in the coordination of attention, we tested whether its strength co-varied with attention-related modulations of local alpha-band amplitudes and behavioral performance.

Section snippets

Participants and recordings

Cortical activity was recorded from 14 healthy participants (mean: 26.4 years old, range: 20–33; seven females) with normal or corrected to normal vision using a 306 channel MEG instrument composed of 204 planar gradiometers and 102 magnetometers (Elekta Neuromag, Helsinki, Finland) at 600 Hz sampling rate. After screening of behavioral results, one participant was excluded from further analysis due to very poor performance (13% detection in the low contrast condition). Maxfilter software

Visual attention improves behavioral performance

We measured MEG data from 14 participants performing a cued visuospatial attention task. Participants were first cued to attend to the left or right visual hemifield after which one of two target shapes was displayed in either hemifield at high (75% discrimination) or low (50% detection) contrast (Fig. 1A). They discriminated and reported shape identity regardless of its location. In the Low Contrast condition, DI-HR was at chance level (∼0.5) while in the high contrast condition, DE-HR was at

Discussion

We used data-driven analyses of source-localized MEG data to assess the role of large-scale phase synchronization of cortical oscillations in anticipatory visuospatial attention. Our study reproduced the commonly observed lateralized suppression of local low-alpha amplitudes in visual cortex. This well-known phenomenon was, however, paralleled by a previously unreported and robust strengthening of inter-areal phase synchronization exclusively in the high-alpha frequency band. High-alpha

Conclusion

We found high-alpha phase synchronization to be associated with anticipatory visuospatial attention. High-alpha synchronization connected the major hubs of DAN, FPN and visual systems while synchronization strength predicted both the behavioral attentional benefit and low-alpha amplitude suppression. High-alpha band synchronization could thus support anticipatory endogenous attention by regulating collective neuronal processing across frontal, parietal and visual cortices and modulating local

Acknowledgements

This study was supported by the Academy of Finland (SA 266402and SA 273807 to S.P. and SA 253130 to J.M.P.). The authors declare no competing financial interests.

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