Elsevier

NeuroImage

Volume 68, March 2013, Pages 112-118
NeuroImage

Coupling between visual alpha oscillations and default mode activity

https://doi.org/10.1016/j.neuroimage.2012.11.058Get rights and content

Abstract

Although, on average, the magnitude of alpha oscillations (8 to 12 Hz) is decreased in task-relevant cortices during externally oriented attention, its fluctuations have significant consequences, with increased level of alpha associated with decreased level of visual processing and poorer behavioral performance. Functional MRI signals exhibit similar fluctuations. The default mode network (DMN) is on average deactivated in cognitive tasks requiring externally oriented attention. Momentarily insufficient deactivation of DMN, however, is often accompanied by decreased efficiency in stimulus processing, leading to attentional lapses. These observations appear to suggest that visual alpha power and DMN activity may be positively correlated. To what extent such correlation is preserved in the resting state is unclear. We addressed this problem by recording simultaneous EEG-fMRI from healthy human participants under two resting-state conditions: eyes-closed and eyes-open. Short-time visual alpha power was extracted as time series, which was then convolved with a canonical hemodynamic response function (HRF), and correlated with blood-oxygen-level-dependent (BOLD) signals. It was found that visual alpha power was positively correlated with DMN BOLD activity only when the eyes were open; no such correlation existed when the eyes were closed. Functionally, this could be interpreted as indicating that (1) under the eyes-open condition, strong DMN activity is associated with reduced visual cortical excitability, which serves to block external visual input from interfering with introspective mental processing mediated by DMN, while weak DMN activity is associated with increased visual cortical excitability, which helps to facilitate stimulus processing, and (2) under the eyes-closed condition, the lack of external visual input renders such a gating mechanism unnecessary.

Highlights

► Recorded simultaneous resting-state EEG-fMRI (both eyes-closed and eyes-open) ► Found positive correlation between visual alpha power and default mode activity ► Functional interpretation provided ► Eyes-open and eyes-closed resting entails different organizations of brain networks.

Introduction

Field oscillations in the alpha range (8–12 Hz) are a prominent feature of human electroencephalogram (EEG) over the occipital–parietal cortex. The genesis and function of alpha have been the subject of intense study since the 1920s (Berger, 1929, Bollimunta et al., 2008, Bollimunta et al., 2011, Lopes da Silva, 1991, Shaw, 2003). It is generally believed that for a given brain state (e.g., attention versus relaxed wakefulness), the magnitude of alpha is an inverse indicator of cortical excitability, with smaller alpha associated with improved visual processing. Goal-oriented increase of alpha over task-irrelevant cortices, therefore, has been interpreted as reflecting a mechanism of active inhibition (Jensen et al., 2002, Klimesch, 1996). In tasks demanding externally-oriented attention, alpha power, on average, is reduced over task-relevant cortices (Rajagovindan and Ding, 2010, Sauseng et al., 2005). Momentary increase of alpha power over these task-relevant cortices is indicative of decreased level of attention and worsened task performance (Macdonald et al., 2011). A recent study examining the neural signature of attention lapses has found increased alpha band oscillation up to 20 s prior to the occurrence of an error (O'Connell et al., 2009).

The level of BOLD activity in the default mode network (DMN), a key system mediating introspective processes such as mind wandering (Christoff et al., 2009, Mason et al., 2007), appears to exhibit behavior similar to that of alpha. It is suppressed or deactivated on average when subjects are actively engaged in demanding cognitive tasks (Buckner et al., 2008). Stronger deactivation of the DMN is associated with greater activation of the sensory cortices (Greicius and Menon, 2004). Attentional lapses, characterized by ineffective stimulus processing and decreased task performance, are associated with momentarily insufficient deactivation of the DMN (Eichele et al., 2008, Weissman et al., 2006).

Based on these functional data, it seems reasonable to expect that alpha power and DMN activity be positively correlated, and this property should persist even in the absence of tasks (resting-state). This hypothesis has been subjected to experimental test using the simultaneous EEG-fMRI technique. Despite repeated attempts (Goldman et al., 2002, Laufs et al., 2003a, Laufs et al., 2003b, Laufs et al., 2006, Moosmann et al., 2003), however, supporting evidence remains lacking. A closer examination of the literature suggests one possible reason, namely, resting-state data were often recorded with the eyes closed. Such data may not be ideally suited to model observations made under conditions of active visual processing. From a functional standpoint, positive alpha and DMN BOLD correlation, implying concurrent increase and decrease of alpha power and DMN BOLD, may serve to gate out sensory input to protect introspective processes from external interference. This protection is only necessary in the presence of visual input. Moreover, the act of opening the eyes has physiological consequences, including some reorganization of brain network activity. In particular, it has been shown that eyes-opening (1) suppresses alpha (Berger, 1929, Moosmann et al., 2003) and (2) increases functional connectivity within DMN (Yan et al., 2009).

In this study we sought to examine the relationship between occipital alpha oscillations and DMN activity by recording simultaneous EEG-fMRI in two types of resting-state sessions: a more traditional eyes-closed session and a less traditional eyes-open session. Alpha power fluctuations were extracted from visual EEG channels using short-time Fourier transforms and convolved with a canonical hemodynamic response function (HRF). The HRF-convolved alpha power time series was then correlated with the concurrent BOLD activity to assess their coupling.

Section snippets

Experimental procedure and data acquisition

Fourteen healthy college students with normal or corrected-to-normal vision participated in the study in exchange of course credit. The experimental protocol and data acquisition procedure were approved by the Institutional Review Board of the University of Florida. Prior to experiment, written informed consent was obtained from all participants.

The experiment consisted of two resting-state fMRI sessions each lasting 7 min. Participants were instructed to remain still, stay awake, not to think

EEG spectra

For a typical subject, from the artifact-free EEG voltage data in Fig. 1A, alpha oscillations are clearly seen in both eyes-closed and eyes-open conditions. At the group level, average power spectra combining the three occipital channels are shown in Fig. 1B, where the mean peak frequency is centered around 10 Hz (eyes-closed: 8.87 ± 1.14 Hz; eyes-open: 9.03 ± 0.85 Hz). The average alpha power under the eyes-open condition was significantly lower than that under the eyes-closed condition (p < 0.05),

Discussion

The coupling between visual alpha oscillations and BOLD activity under both eyes-closed and eyes-open resting-state conditions was considered. Consistent with previous reports, the posterior alpha power was negatively correlated with BOLD activity in a frontoparietal network (Laufs et al., 2003a, Laufs et al., 2003b), and this negative correlation was further found to be not affected by whether eyes were open or closed. Positive alpha-BOLD correlation was found only for the eyes-open condition

Acknowledgment

This work was supported by NIH R01 grant MH097320.

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