Sensory gating of auditory evoked and induced gamma band activity in intracranial recordings

Abstract

Oscillatory activity in the gamma band range (30–50 Hz) and its functional relation to auditory evoked potentials (AEPs) is yet poorly understood. In the current study, we capitalized on the advantage of intracranial recordings and studied gamma band activity (GBA) in an auditory sensory gating experiment. Recordings were obtained from the lateral surface of the temporal lobe in 34 epileptic patients undergoing presurgical evaluation. Two kinds of activity were differentiated: evoked (phase locked) and induced (not phase locked) GBA. In 18 patients, an intracranial P50 was observed. At electrodes with maximal P50, evoked GBA occurred with a similar peak latency as the P50. However, the intensities of P50 and evoked GBA were only modestly correlated, suggesting that the intracranial P50 does not represent a subset of evoked GBA. The peak frequency of the intracranial evoked GBA was on average relatively low (∼25 Hz) and is, therefore, probably not equivalent to extracranially recorded GBA which has normally a peak frequency of ∼40 Hz. Induced GBA was detected in 10 subjects, nearly exclusively in the region of the superior temporal lobe. The induced GBA was increased after stimulation for several hundred milliseconds and encompassed frequencies up to 200 Hz. Single-trial analysis revealed that induced GBA occurred in relatively short bursts (mostly ≪100 ms), indicating that the duration of the induced GBA in the averages originates from summation effects. Both types of gamma band activity showed a clear attenuation with stimulus repetition.

Introduction

Sensory gating refers to the basic ability of the brain to suppress the response to repeated (and possibly irrelevant) environmental stimuli (Venables, 1964). The typical experimental setup for electrophysiological studies of sensory gating in the auditory domain applies pairs of clicks, separated by a short interstimulus interval (ISI, 0.5 s) and a long interpair interval (8–12 s) (Adler et al., 1982). Healthy control subjects have on average reduced P50 amplitudes as response to the second stimulus, as compared to the P50 elicited by the first stimulus. This amplitude reduction or suppression is regarded as an indicator of sensory gating (Nagamoto et al., 1991).

Most studies on sensory gating are restricted to the analysis of the P50, although there were some studies investigating also the suppression of later auditory evoked potential (AEP) components (Boutros et al., 2004) and the suppression of the evoked gamma band activity (GBA) (Clementz et al., 1997). In neuromagnetic recordings, such an evoked (or phase-synchronized) GBA with a maximum at 40 Hz was reported to occur in a latency range of 30–100 ms (Pantev et al., 1991). GBA is of particular interest in neuroscience research as it has been linked to a variety of perceptual and cognitive functions such as feature binding, object representation or selective attention (Bertrand and Tallon-Baudry, 2000, Engel and Singer, 2001, Fell et al., 2003, Keil et al., 2001, Tiitinen et al., 1993, Varela et al., 2001). Alterations in GBA have also been related to pathological processes (Lee et al., 2003, Llinas et al., 1999).

The P50 and the evoked GBA are difficult to separate because they overlap in the time and frequency domain. It has even been proposed that P50 and evoked GBA represent the same phenomenon (Basar et al., 1987, Clementz et al., 1997). The AEP is typically filtered from 10 to 50 Hz for the study of the P50 and from 30 to 50 Hz for the study of the evoked GBA. Furthermore, the study of GBA and P50 in surface recordings is handicapped by small signal amplitudes and possible contamination with high-frequency muscle artefacts. Intracranial recordings avoid an attenuation of the EEG signal by intervening tissues between the cortical generators and surface electrodes particularly in the higher frequency range (Pfurtscheller and Cooper, 1975) and might, therefore, be regarded as ideally suited for the investigation of GBA. However, the opportunity for intracranial recordings in humans is rare and restricted to presurgical evaluation of epilepsy and tumor patients.

In a study on epilepsy patients, GBA elicited by visual stimuli was recorded intracranially while patients performed a Kanizsa task (Lachaux et al., 2000). Interestingly, besides evoked GBA, induced (not phase-synchronized) GBA was observed, occurring in a time range from 200 to 500 ms. Similarly, both kinds of GBA were also recorded from the temporal lobe after auditory stimulation with tones and phonemes (Crone et al., 2001). In this study, power changes in GBA were analyzed in recordings from 4 subjects with tones and phonemes as stimuli. As a major finding, induced GBA was assumed to be confined not only to the well-known GBA at about 40 Hz but also comprised activity of considerably higher frequencies (80–100 Hz). The induced GBA started at about the same time as the invasively recorded N100 but outlasted this component. Topographically, it was found adjacent to electrode sites with a prominent N100 peak, but its topographical distribution was not identical to that of the N100. Induced GBA after acoustic stimulation was also observed in monkeys (Brosch et al., 2002).

The current investigation was conducted within the framework of a larger study on a functional neuroanatomical model of sensory gating. In general, this study targets to describe neuronal correlates of sensory gating by intracranial recordings in humans. Here, we investigated the occurrence of evoked and induced GBA in a typical sensory gating experiment with paired clicks. The first aim of the study was to examine whether evoked GBA can be observed at intracranial leads and compare such an evoked GBA to characteristics of P50. The second aim was to prove whether induced GBA is elicited also by the very short stimuli with a duration of a few milliseconds only, as usually applied in sensory gating experiments. Finally, the effect of stimulus repetition was assessed for evoked and induced GBA as well as for the AEP components P50 and N100. For these purposes, brain signals were analyzed in the time–frequency domain by wavelet transform.