Gamma and beta frequency oscillations in response to novel auditory stimuli: A comparison of human electroencephalogram (EEG) data with in vitro models

Abstract

Investigations using hippocampal slices maintained in vitro have demonstrated that bursts of oscillatory field potentials in the gamma frequency range (30 -80 Hz) are followed by a slower oscillation in the beta 1 range (12-20 Hz). In this study, we demonstrate that a comparable gamma-to-beta transition is seen in the human electroencephalogram (EEG) in response to novel auditory stimuli. Correlations between gamma and beta 1 activity revealed a high degree of interdependence of synchronized oscillations in these bands in the human EEG. Evoked (stimulus-locked) gamma oscillations preceded beta 1 oscillations in response to novel stimuli, suggesting that this may be analogous to the gamma-to-beta shift observed in vitro. Beta 1 oscillations were the earliest discriminatory responses to show enhancement to novel stimuli, preceding changes in the broad-band event-related potential (mismatch negativity). Later peaks of induced beta activity over the parietal cortex were always accompanied by an underlying gamma frequency oscillation as seen in vitro. A further analogy between in vitro and human recordings was that both gamma and beta oscillations habituated markedly after the initial novel stimulus presentation.

Gamma and beta neural activity evoked during a sensory gating paradigm: Effects of auditory, somatosensory and cross-modal stimulation

“…If such a pattern were not observed, it would be difficult to rule out the possibility that reduced amplitude beta response as a function of reduced ISI simply reflects global cortical refractoriness. We did not expect this more trivial explanation for dependence of beta response on ISI to be applicable here: within-modality changes in stimulus identity (e.g., a change in the frequency of auditory tones), even at fixed ISI, has been shown to produce increased beta response amplitude (Haenschel et al, 2000). A similarly robust dishabituation of event-related gamma-band activity by changing stimulus identity at short ISI was not expected here: even when stimuli are presented at short ISI, obligatory stimulus processing should not depend upon the physical match or mismatch to the preceding stimulus.…”

“…Although C3′ is commonly employed for measurement of somatosensory potentials, Cz was used here across all conditions (including somatosensory and combined) in order to allow for comparison of response between modalities (see also Arnfred et al, 2001a). Electrode Fz was included because Haenschel et al (2000) showed that stimulus-evoked oscillatory activity is strongly modulated by stimulus-driven salience across fronto-central sites. Although originally included in the analyses, Fz was dropped from the current presentation because there was not substantial difference between activity -including modulation of activity by ISI -at this electrode and the nearby Cz site.…”

“…This transition did not occur after stimulation at lower stimulus intensities, although the gamma rhythm was still observed. Scalp-recorded electroencephalographic measures of neuron population activity in the intact human brain have been shown to exhibit a similar pattern of response to stimulusdriven salience: Haenschel et al (2000) demonstrated that an evoked gamma band response was followed by a robust beta band response, but only when the auditory stimulus suddenly changed from the ongoing acoustic background. This apparent gamma-to-beta transition occurred within 150 ms of stimulus onset in response to these high salience stimuli.…”

“…This apparent gamma-to-beta transition occurred within 150 ms of stimulus onset in response to these high salience stimuli. Thus, although Traub et al (1999) and Haenschel et al (2000) employed substantively different neurophysiological measures of neuron population activity, and although they operationalized "salience" differently, they both highlighted the sensitivity of evoked beta band activity to stimulus-driven salience.…”

“…Whereas in vitro studies have typically investigated oscillations that are not necessarily phase-locked to a stimulus (i.e., induced), Haenschel et al (2000) found that only the early (20-150 ms) phase-locked oscillations exhibit the expected gamma-to-beta transition pattern in response to high salience stimuli for scalprecorded measures of intact human brain activity. Later (200-400 ms) induced oscillations were detected in that study, but beta activity preceded gamma activity in that latency window.…”