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Gamma and beta frequency oscillations in response to novel auditory stimuli: A comparison of human electroencephalogram (EEG) data with in vitro models Corinna Haenschel*†, Torsten Baldeweg‡, Rodney J. Croft*, Miles Whittington§, and John Gruzelier* *Division of Neuroscience and Psychological Medicine, Imperial College School of Medicine, London W6 8RP, United Kingdom; ‡Institute of Child Health and Great Ormond Street Hospital for Sick Children, University College London, London WC1N 2AP, United Kingdom; and §School of Biomedical Sciences, University of Leeds, Leeds LS2 9NL, United Kingdom Communicated by Nancy J. Kopell, Boston University, Boston, MA, April 10, 2000 (received for review December 15, 1999) Investigations using hippocampal slices maintained in vitro have neuronal assembly within which synchronization is possible (11). demonstrated that bursts of oscillatory field potentials in the This observation is complementary to the demonstration that gamma frequency range (30–80 Hz) are followed by a slower long-range (multimodal) sensory coding is performed at beta oscillation in the beta 1 range (12–20 Hz). In this study, we frequencies, whereas local synchronization occurs at gamma demonstrate that a comparable gamma-to-beta transition is seen frequencies (12). in the human electroencephalogram (EEG) in response to novel Transient bursts of gamma oscillations in the human electro- auditory stimuli. Correlations between gamma and beta 1 activity encephalogram (EEG) can be detected in response to sensory revealed a high degree of interdependence of synchronized oscil- stimulation (13). They can either be tightly time and phase lations in these bands in the human EEG. Evoked (stimulus-locked) locked to the stimulus (termed stimulus-evoked gamma oscilla- gamma oscillations preceded beta 1 oscillations in response to tions) (14), or they may occur with variable latency (termed novel stimuli, suggesting that this may be analogous to the stimulus-induced gamma oscillations) (15). Stimulus-evoked gamma-to-beta shift observed in vitro. Beta 1 oscillations were the gamma oscillations are contained in the averaged evoked po- earliest discriminatory responses to show enhancement to novel tential and can be extracted by band-pass filtering (14). Such short-latency gamma-band oscillations have been found in the stimuli, preceding changes in the broad-band event-related poten- auditory potential within 100 ms from stimulus onset (16–19). In tial (mismatch negativity). Later peaks of induced beta activity over contrast, stimulus-induced gamma oscillations disappear in the the parietal cortex were always accompanied by an underlying average evoked potential because of the jitter in latency from gamma frequency oscillation as seen in vitro. A further analogy one trial to the next. They have to be extracted by using methods between in vitro and human recordings was that both gamma and that distinguish between phase-locked and non-phase-locked beta oscillations habituated markedly after the initial novel stim- activity (20). In this study, we used the method of event-related ulus presentation. synchronization and desynchronization (21). Induced gamma activity has been found in response to sensory PSYCHOLOGY amma and beta frequency oscillations occur in the neocor- stimuli in the human EEG (15, 20). The functional significance Gtex in response to sensory stimuli over a range of modalities of evoked and induced gamma oscillations still remains unclear. (1, 2). Evidence is accumulating that gamma oscillations are However, it has been suggested that the evoked gamma band involved in feature binding and associational memory (3, 4). The response may reflect synchronously active neural assemblies mechanism behind these cortical oscillations remains to be (feature binding) or may signal the precise temporal relationship elucidated, but research has demonstrated that, at a cellular and of concurrently incoming stimuli (20). The later induced gamma network level, cortical gamma activity can be generated by oscillation is thought to reflect object representation (3, 20) or specific neuronal subtypes (5) and networks of interconnected the activation of associative memories (4, 22). Recent in vitro studies have demonstrated that stimulus- inhibitory interneurons (6). At a larger network level, focal induced gamma and beta oscillations habituate markedly on cortical gamma oscillations can be elicited upstream from pri- repeated stimulation (23). The aim of this study was to investi- mary sensory pathways by tetanic stimulation of the thalamic gate the relationship between gamma and beta oscillations in the reticular nucleus (7). Previous studies using cortical and hip- human EEG in response to novel and repeated auditory stimuli pocampal slice preparations have demonstrated that experimen- designed to mimic the in vitro paradigm. We tested the hypoth- tal gamma oscillations can occur spontaneously for long periods esis that novel stimuli differing in frequency from a repeated of time during activation of metabotropic cholinergic receptors sequence of tones would elicit a similar burst of correlated (8) and can be induced transiently by activation of metabotropic gamma and beta 1 activity. Furthermore, we expected that these glutamate receptors or by bursts of afferent stimulation (6, 9, 10). responses, particularly with regard to induced oscillations, would Experimentally, beta frequency oscillations are generated habituate rapidly with stimulus repetition. following periods of synchronous gamma frequency activity (9, 10). Their generation depends on the period-by-period poten- Methods tiation of recurrent excitatory synaptic potentials, which occurs Subjects. Ten participants (three females, seven males), 20–35 concurrently with a recovery of postspike afterhyperpolarization years old (mean, 21.5), with normal hearing were tested. All following the initial stimulus. The beta oscillations appeared to manifest as subharmonics of the preceding gamma oscillation, with pyramidal cells firing on only every second or third period Abbreviations: EEG, electroencephalogram; ERP, event-related potential; GFP, global field of a continuing subthreshold, inhibition-based gamma oscilla- power; MMN, mismatch negativity. †To whom reprint requests should be addressed at: Cognitive Neuroscience and Behavior, tion. As a consequence, all cells involved in the beta network will Imperial College School of Medicine, London W6 8RP, UK. E-mail: [email protected]. skip the same beats. These oscillations have been suggested to The publication costs of this article were defrayed in part by page charge payment. This represent a dynamic method of generating and recalling stimu- article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. lus-specific assemblies of neurons. In addition, recent efforts to §1734 solely to indicate this fact. model beta oscillations have shown that their generation en- Article published online before print: Proc. Natl. Acad. Sci. USA, 10.1073͞pnas.120162397. hances the range of temporal delays between elements in a Article and publication date are at www.pnas.org͞cgi͞doi͞10.1073͞pnas.120162397 PNAS ͉ June 20, 2000 ͉ vol. 97 ͉ no. 13 ͉ 7645–7650 Downloaded by guest on September 28, 2021 participants were free of neurological and psychiatric disorders (Neuroscan Labs) based on the method of complex demodula- and had no history of hearing impairment. Ethical approval was tion (25, 26). First, the center frequency (CF) and cut-off obtained and all participants provided written consent before frequency were selected for a zero-phase bandpass filter. Com- testing. Subjects were seated in an armchair with head support plex demodulation then produced a complex time series [with in a sound-attenuated and electrically shielded testing chamber. real part cos(2␲⅐CF⅐t) and imaginary part sin(2␲⅐CF⅐t)] from the Instructions were given to relax completely with eyes closed. original real-time series. This had the effect of shifting the entire spectrum of the original time series to 0 Hz. Both the real and Stimuli. Pure sinusoidal tones were generated with a Neurosoft imaginary parts were low-pass filtered. Then the envelope of the Sound program and delivered binaurally through headphones by center frequency activity was computed as the modulus of the the Stim interface system (Neuroscan Labs, Sterling, VA). complex time series after filtering (in units of power in ␮V2). To Stimuli were presented in a series of 40 trials. A single trial compute the induced band power statistic across all epochs, the consisted of a sequence of 8 tones (randomized up to a maximum modulus squared was summed across all epochs, and the real and of 16) of one constant frequency, of which the first eight were imaginary parts were summed across all epochs (at each time analyzed. The tone frequency altered randomly between trials point within the epoch). The mean across epochs at each time from the lower frequency limit of 100 Hz to the upper limit of point (average evoked potential) was explicitly removed for the 5000 Hz (from 100 to 1000 Hz in steps of 100 Hz and between power computations. The result is the event-related induced 1000 and 5000 Hz in steps of 200 Hz). The tones were 50 ms long band power. Mean and peak amplitude as well as latency of the (rise and fall time 5 ms), had an intensity of 95 dB (sound induced oscillations were identified in the time window between pressure level), and were presented with a constant stimulus 200 and 400 ms and 600

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