Elsevier

Brain Research

Volume 1232, 26 September 2008, Pages 163-172
Brain Research

Research Report
Cross-frequency phase coupling of brain rhythms during the orienting response

https://doi.org/10.1016/j.brainres.2008.07.030Get rights and content

Abstract

A critical function of the brain's orienting response is to evaluate novel environmental events in order to prepare for potential behavioral action. Here, measures of synchronization (power, coherence) and nonlinear cross-frequency phase coupling (m:n phase locking measured with bicoherence and cross-bicoherence) were computed on 62-channel electroencephalographic (EEG) data during a paradigm in which unexpected, highly-deviant, novel sounds were randomly intermixed with frequent standard and infrequent target tones. Low frequency resolution analyses showed no significant changes in phase coupling for any stimulus type, though significant changes in power and synchrony did occur. High frequency resolution analyses, on the other hand, showed significant differences in phase coupling, but only for novel sounds compared to standard tones. Novel sounds elicited increased power and coherence in the delta band together with m:n phase locking (bicoherence) of delta:theta (1:3) and delta:alpha (1:4) rhythms in widespread fronto-central, right parietal, temporal, and occipital regions. Cross-bicoherence revealed that globally synchronized delta oscillations were phase coupled to theta oscillations in central regions and to alpha oscillations in right parietal and posterior regions. These results suggest that globally synchronized low frequency oscillations with phase coupling to more localized higher frequency oscillations provide a neural mechanism for the orienting response.

Introduction

The orienting response is a fundamental biological mechanism that is necessary for survival (Luria, 1973). It is a rapid response to new, unexpected or unpredictable events that entails the involuntary (so-called “bottom up”) capture of attention and essentially functions as a “what-is-it” detector (Sokolov, 1990). The neural correlates of the orienting response in humans have been most often studied by recording event-related potentials (ERPs) during the auditory novelty oddball paradigm. In that paradigm, stimuli consist of a frequent tone (the standard) randomly interspersed with less frequent target tones and novel sounds. The latter are a set of unexpected environmental sounds that occur only once per experiment. A great deal of research has indicated that the P3 component of the ERP elicited by novel sounds is an electrophysiological correlate of the orienting response (Friedman et al., 2001). This novelty P3 (called P3a) is distinct from the P3 elicited by equally-infrequent targets tones (called P3b) in its cognitive correlates, surface topography and intracranial sources. Widespread posterior, parietal, and temporal areas contribute to the P3b and widespread frontal, parietal, and temporal areas contribute to the P3a (Friedman et al., 2001, Ranganath and Rainer, 2003). These electrophysiological studies of the orienting response have primarily been carried out in the time domain by analyzing amplitudes, latencies, and intracranial source models of ERP components. Complementary analysis of EEG recordings in the frequency domain makes it possible to directly quantify known neural mechanisms such as synchronization and cross-frequency coupling of field potential oscillations (Isler et al., 2007). Such analyses provide a framework to investigate how the distributed neuronal networks that underpin the orienting response act in concert to determine what the deviant, environmental perturbation represents, evaluate its significance, and prepare for a possible behavioral response.

Synchronization of oscillations in electric field potentials within and between brain regions is an efficient mechanism for coalescing local and regional assemblies into more widespread networks (Varela et al., 2001). Oscillatory synchrony can function as a fundamental mechanism in both perception (Gray et al., 1989, Tallon-Baudry et al., 1996) and behavior control (Pfurtscheller et al., 1994, von Stein et al., 2000). Membrane potential oscillations precipitate plasticity (LTP/LTD) even in the absence of post-synaptic action potentials, i.e. without Hebbian plasticity (Golding et al., 2002). Furthermore, at least for some brain rhythms and regions, information is encoded in the phase of oscillatory activity (O'Keefe and Recce, 1993). Phase encoding offers a rich modality for “putting oscillations to work” in the brain and has been proposed as a potential mechanism for working memory (Buzsaki, 2005; Jensen and Lisman, 1998). We hypothesized that it could be a brain mechanism for the orienting response.

Increasingly, there is evidence that oscillations in the traditional EEG frequency bands (delta 1–4 Hz, theta 4–8 Hz, alpha 8–12 Hz, beta 12–25 Hz, gamma > 25 Hz) are manifestations of, and may even facilitate, different cognitive functions (Buschman and Miller, 2007; Buzsaki and Draguhn, 2004), although the mapping from function to frequency may not be unique and may be dynamically and spatially variable (Palva and Palva, 2007). For example, the theta band is associated with memory and information transfers between neocortex and hippocampus (Kahana et al., 2001) while the gamma band is associated with stimulus feature binding, localized representations, and awareness (Bertrand and Tallon-Baudry, 2000, Lachaux et al., 2000, Rodriguez et al., 1999). Consequently, coupling of oscillatory activity across frequency bands (cross-frequency coupling) provides a simple mechanism whereby distinct cognitive functions can operate conjointly to perform a given task (Jensen and Colgin, 2007). Cross-frequency coupling in which the amplitude of one frequency is modulated by the phase of another frequency (phase-amplitude coupling) has been observed in intracortical recordings (Canolty et al., 2006) in both spontaneous and task-related activity and has led to the idea of an oscillatory hierarchy made up of nested phase-amplitude relationships (Lakatos et al., 2005). Another form of cross-frequency coupling is phase-phase coupling (or m:n phase locking, or simply phase coupling) which occurs as the result of nonlinear interactions between frequencies, though it can also arise due to nonlinear distortions, autoresonance, and other nonlinear processes. Demonstration of this form of coupling has been made in vitro (Gloveli et al., 2005) and in vivo (Palva et al., 2005, Schack et al., 2002). With phase coupling, information encoded in the phase of the higher frequency is preserved across multiple cycles of the lower frequency rhythm. This provides a mechanism for multiplexing the activity in a single neuron or local neuronal population because the same neuron(s) can simultaneously phase-encode at multiple frequencies.

The goal of the present study was to determine if cross-frequency phase coupling of electric potential oscillations occurs as part of the brain's orienting response to unexpected environmental stimuli. We hypothesized that it would, under the assumption that neuronal networks exhibiting synchronized oscillations at different frequencies (perhaps subserving distinct cognitive functions) would be interacting during the orienting response. We tested our hypothesis by quantifying synchronizaton and cross-frequency phase coupling of brain oscillations in the auditory novelty oddball paradigm. Specifically, we hypothesized that cross-frequency phase coupling would be greater for novel sounds than for target and standard tones. Furthermore, we expected regional synchronization to be greater for target than standard tones, and even greater for novel sounds than targets, with a spatial distribution that was more anterior for novels and more posterior for targets.

Section snippets

Results

Fig. 1 shows grand-averaged waveforms for frontal (Fz, top) and posterior electrodes (Pz, bottom) for the three stimulus types. As in previous studies, all three stimuli elicit a P1–N1–P2 complex at early latencies (< 200 ms) while novel sounds elicit a large positive potential over frontal regions at approximately 300 ms post-stimulus whereas target tones elicit a somewhat later and broader positive potential over posterior regions (Friedman et al., 2001). Frequency-domain measures of synchrony

Discussion

We hypothesized that cross-frequency phase coupling of electric field potential oscillations would occur for novel environmental sounds but not for target and standard tones in an auditory novelty oddball experiment. In support of our hypothesis, there was widespread coupling of delta:theta and delta:alpha rhythms for novel sounds compared to standard tones, but no significant coupling was observed for targets compared to standards. The lack of coupling in the latter case suggests that

Subjects

The subjects were 13 normal right-handed older adults (5 male) aged 54 to 83 (mean 72) who provided informed consent in accord with the Institutional Review Board at the New York State Psychiatric Institute. This was a secondary analysis of a dataset studying aging. We used this dataset because it offered sufficient power to test our hypotheses and not as a study of aging per se.

Protocol, recording, pre-processing

Subjects were seated in a sound-damped, electrically-shielded room. Sound trains were presented in 10 blocks (80

Acknowledgments

National Institutes of Health (NINDS 5K25NS052230 to J.I., NIA AG005213 to D.F.).

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