Elsevier

NeuroImage

Volume 60, Issue 1, March 2012, Pages 384-391
NeuroImage

Resting oscillations and cross-frequency coupling in the human posteromedial cortex

https://doi.org/10.1016/j.neuroimage.2011.12.019Get rights and content

Abstract

Using rare intracranial recordings from the posterior interhemispheric region of the human brain, we explored the oscillatory properties of the posteromedial cortex (PMC) during rest. The PMC is a core structure of the default mode network, which is known for its higher activity during the resting state. We found that resting PMC spectral power peaked in the theta band range (4–7 Hz) and was clearly distinguishable from adjacent cortical sites in the occipital lobe displaying peaks in the alpha band range (8–12 Hz). Additionally, the phase of PMC theta oscillations modulated the amplitude of ongoing high gamma (70–180 Hz) activity during the resting state. The magnitude of this cross-frequency modulation was shown to fluctuate at time scales comparable to those observed in functional neuroimaging studies of intrinsic functional connectivity networks (~ 0.1 Hz). The difference of canonical oscillations in the PMC compared to its adjacent cortical sites conforms to functional specialization across anatomical boundaries. Such differences may reflect separate oscillatory preferences between networks that are functionally connected.

Highlights

► Human posteromedial cortex (PMC) is the hub of default mode network. ► PMC displays strong theta band (3–7 Hz) oscillations at rest. ► Phase of PMC resting theta modulates the amplitude of high gamma activity. ► Theta/gamma cross-frequency modulation displays slow fluctuations at ~ 0.1 Hz.

Introduction

During the resting state, oscillations of differing peak frequencies predominate across the cerebral cortex. The occipital alpha and the rolandic beta rhythms are classical examples of such canonical oscillations (Adrian and Matthews, 1934, Jasper and Penfield, 1949). More recently, there has been growing evidence for the role of canonical oscillations in modulating local cortical activation and distal cortical interaction through phase-amplitude and phase-phase coupling, respectively (Canolty and Knight, 2010).

Similarly, functional magnetic resonance imaging (fMRI) studies have also revealed unique spatio-temporal patterns of resting state activity, in the form of intrinsic functional connectivity (resting state networks), which reflect correlations in hemodynamic signals at slow time scales (< 1 Hz) (Deco et al., 2011). The default mode network (DMN) is a consistently identified resting state network, of which the posteromedial cortex (PMC) forms the central functional-anatomic node (Buckner et al., 2008, Hagmann et al., 2008). However, despite great research interest, little is known about the electrophysiological properties unique to the PMC, in contrast to adjacent sensory regions, during the resting state. Central to this limitation is the difficulty in obtaining electrophysiological interhemispheric recordings from the PMC in conscious human subjects.

Typically the DMN, and the PMC in particular, is described as having higher blood oxygenation level dependent (BOLD) resting activity which deactivates during attentionally demanding cognitive tasks (Fox et al., 2005). Consistent with these fMRI findings, single-unit recordings in non-human primates (Hayden et al., 2009, Hayden et al., 2010) and intracranial recordings from human subjects (Dastjerdi et al., 2011, Jerbi et al., 2010, Miller et al., 2009, Ossandon et al., 2011) also show clear support for higher activity in PMC during rest, which is suppressed during tasks of external attention. These data suggest resting activation and task deactivation to be best tracked by power shifts in a broad gamma range at the cortical surface (Dastjerdi et al., 2011, Jerbi et al., 2010, Miller et al., 2009, Ossandon et al., 2011). More generally, electrophysiological investigations outside of the DMN have suggested that modulation in gamma amplitude at slower frequencies, similar to those observed in fMRI data, correlate at spatial scales relevant to the study of resting state brain networks (Leopold et al., 2003, Nir et al., 2008).

In the current study, we go beyond the event related changes of gamma activity in the PMC during cued rest fixation (Dastjerdi et al., 2011). We use intracranial recordings in human subjects to measure the signature of electrophysiological activity within the PMC during spontaneous rest. During this state, we show that theta oscillations predominate in PMC and also modulate ongoing gamma amplitude, which distinguishes this region from other nearby areas such as the visual cortex whose activity is preferentially influenced by canonical alpha, rather than theta, oscillations. Additionally, we show that cross-frequency amplitude modulation for the same frequencies fluctuates at slow time scales akin to those observed for resting state networks with fMRI BOLD signals.

Section snippets

Subjects

Direct electrocortical recordings during periods of awake resting state were obtained from subjects implanted with subdural electrodes. Intracranial recordings were performed for clinical reasons related to the surgical treatment of refractory epilepsy. All subjects provided voluntary written consent to participate in research recordings as part of a protocol approved by the Stanford Institutional Review Board office. Results reported here were obtained from 4 subjects (3 female) with electrode

Results

The first finding of our study suggests that the PMC can be distinguished from its nearby cortical regions in terms of its oscillatory properties at rest. As shown in Fig. 1, PMC has a clear spectral peak in the theta range (5 Hz), in contrast to sites in visual cortex of the same subject that show a strong alpha resonance (8 Hz). Furthermore, the PMC shows maximal PAC between theta band phase and HG amplitude while electrodes in the lateral and mesial visual cortex show a clear PAC relationship

Significant findings

Using direct intracranial recordings from the human PMC, we made the following observations: 1) within the PMC there is a predominance of theta oscillations, peaking in the 4–5 Hz range, during the resting state; 2) This differentiates the PMC from its neighboring visual cortices that oscillate in the alpha range during the resting state; 3) the amplitude of ongoing resting HG activity within the PMC is modulated to be maximal at the theta wave trough; 4) the power of theta-modulated high gamma

Acknowledgements

We thank Bradley Voytek for open code sharing; Kai Miller, Dora Hermes, Mohammad Dastjerdi and Christopher Honey for helpful comments. This study was funded by a seed grant from Stanford University Institute of Medicine and the Stanford Institute for NeuroInnovation and Translational Neurosciences (SINTN).

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