Potentials evoked by chirp-modulated tones: a new technique to evaluate oscillatory activity in the auditory pathway

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Abstract

Objective: Steady-state potentials are oscillatory responses generated by a rhythmic stimulation of a sensory pathway. The frequency of the response, which follows the frequency of stimulation, is maximal at a stimulus rate of 40 Hz for auditory stimuli. The exact cause of these maximal responses is not known, although some authors have suggested that they might be related to the ‘working frequency’ of the auditory cortex. Testing of the responses to different frequencies of stimulation may be lengthy if a single frequency is studied at a time. Our aim was to develop a fast technique to explore the oscillatory response to auditory stimuli, using a tone modulated in amplitude by a sinusoid whose frequency increases linearly in frequency (‘chirp’) from 1 to 120 Hz.

Methods: Time-frequency transforms were used for the analysis of the evoked responses in 10 subjects. Also, we analyzed whether the peaks in these responses were due to increases of amplitude or to phase-locking phenomena, using single-sweep time-frequency transforms and inter-trial phase analysis.

Results: The pattern observed in the time-frequency transform of the chirp-evoked potential was very similar in all subjects: a diagonal band of energy was observed, corresponding to the frequency of modulation at each time instant. Two components were present in the band, one around 45 Hz (30–60 Hz) and a smaller one between 80 and 120 Hz. Inter-trial phase analysis showed that these components were mainly due to phase locking phenomena.

Conclusions: A simultaneous testing of the amplitude-modulation-following oscillatory responses to auditory stimulation is feasible using a tone modulated in amplitude at increasing frequencies. The maximal energies found at stimulation frequencies around 40 Hz are probably due to increased phase-locking of the individual responses.

Introduction

Cortical oscillatory activity may be a key mechanism in perceptual binding (Singer, 1993). The role of synchronous oscillations in perception has been suggested by studies performed at very different levels, from single neuron activity to EEG and MEG (Engel et al., 1992, Tallon-Baudry et al., 1996, Rodriguez et al., 1999). These two latter techniques are limited by the spatial filter imposed by the head, although they have the invaluable advantage of being non-invasive.

There are several approaches to the study of cortical oscillatory activity using EEG. An oscillatory response to a stimulus may have a constant phase relationship with it (phase-locked or ‘evoked’ response) or may consist of a change in the amplitude in the ongoing activity without a clear phase relationship with the stimulus (non phase-locked or ‘induced’ response) (Pfurtscheller and Lopes da Silva, 1999). The most typical examples of phase-locked responses are the evoked potentials. There are two possible mechanisms that can generate an evoked potential in an averaged response. It can result from the sum of low-amplitude potentials generated in each individual sweep; with the averaging process, the amplitude of the background EEG noise is reduced and these low-amplitude potentials come up and can be clearly observed. Alternatively, these responses might be due to synchronous phase-resetting in the ongoing activity caused by the stimulus, without any amplitude changes (Başar et al., 1992, Makeig et al., 2002, Penny et al., 2002).

Steady-state responses (SSRs) are the result of averaging individual responses to trains of rhythmic stimuli delivered at a constant frequency (so the ‘steady-state’ name) (Stapells et al., 1984). They have a frequency content which is maximum at the frequency of stimulation.

SSRs have been obtained with auditory and visual stimuli. Auditory steady-state responses were initially described with trains of clicks (Galambos et al., 1981), but they can also be obtained with amplitude-modulated (AM) tones (Picton et al., 1987). The amplitude of the oscillations is maximal at stimulation frequencies around 40 Hz (30–50 Hz) (Galambos et al., 1981), with a second component of smaller amplitude between 80 and 120 Hz (Lins et al., 1995). The cause of the maximal response at stimulation rates around 40 Hz has been intensely debated; it is not clear whether it is just due to the superposition of the middle latency responses to each single stimulus or there is some kind of resonance phenomena in the auditory pathway at that frequency (John and Picton, 2000). In this latter case, the frequency of the maximal response could indicate the preferential working frequency of the auditory network. An alteration in the brain ‘working frequencies’ has been hypothesized as a possible cause of some neurological disorders (McCormick, 1999).

If one modulation frequency is used at a time, testing the SSRs to different stimulation frequencies can be very long, depending on the number of frequencies to examine. A faster approach has been proposed, both for visual and auditory steady-state responses, with the help of a Fourier analyzer (Regan, 1977, Stapells et al., 1984).

Our purpose was to prove the feasibility of a test that allows the simultaneous study of the auditory steady-state responses to many different frequencies of stimulation, using a tone modulated in amplitude at increasing frequencies from 1 to 120 Hz (‘chirp’). As a secondary endpoint, our study tried to establish whether the higher amplitude of the frequency-following responses around 40 Hz is due to an increase in the amplitude of the response at this frequency or to an increase in the inter-trial phase-locking.

Section snippets

Subjects and methods

Twelve young healthy subjects were initially included in the study. All of them were informed in detail about the experiment, and gave their written consent. Two subjects were excluded ‘a posteriori’ from the analysis, one of them due to a previously undocumented partial hearing loss in the range of the carrier tone, and another due to a high-amplitude muscle artifact. Therefore, only 10 subjects were included in the final analysis. The protocol was approved by the institutional ethics

Steady-state responses

The average of the responses yielded in all subjects an oscillatory potential with several components (Fig. 2, top left). Although some oscillatory changes were already present in some subjects in partial averages of as few as 30 sweeps, the signal-to noise ratio and the amplitude of the changes increased steadily up to 400–500 sweeps per subject. An initial response, consisting of two consecutive N1-P2 complexes, was observed about 120 ms after the beginning of the sound (mean latency for the

Chirp-evoked potentials as a new test

Our results have shown that it is possible to analyze the oscillatory response to different frequencies of stimulation in a simultaneous way using the time-frequency transform of the potential evoked by a chirp-modulated tone (a tone modulated in amplitude at increasing frequencies). With this technique, the frequency at which the maximum response is obtained, as well as the range of frequencies in which there is an oscillatory response, can be easily determined. The results obtained are

Acknowledgements

This work has been supported by grant 030043 from the Fondo de Investigaciones Sanitarias, Spain.

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