Effects of tone repetition on auditory evoked neuromagnetic fields

https://doi.org/10.1016/j.clinph.2003.11.011Get rights and content

Abstract

Objective: To investigate the impact of stimulus repetition on neuromagnetic auditory evoked fields (AEF) in the context of permanently varying auditory stimulation and uniform stimulation.

Methods: Left-hemispheric AEF of 16 healthy subjects were recorded on a 31-channel system. In one condition subjects were stimulated with trains of 5 identical tones, in another condition the pitch of the stimuli varied from 800 to 1250 Hz in 50 Hz steps and every 10th stimulus was followed by an identical stimulus. Evoked cortical activity was estimated by calculation of the signal:noise ratio and by dipole reconstruction.

Results: If the stimuli were permanently varied, tone repetition elicited a neuromagnetic mismatch negativity (MMNm) in about half of the subjects, while the AEF component N100m was not significantly affected. If trains of uniform stimuli were applied, a significant decrease of the N100m dipole moment was observed from the first to the second stimulation only. The N100m dipole location in mediolateral direction, however, varied at least between the first 3 stimulus positions.

Conclusions: An MMNm can be elicited by tone repetition even at interstimulus intervals extending the so-called temporal window of integration. The data on repeated stimulation with uniform tones reveal a dissociation between effects on N100m dipole moment and location.

Introduction

The cortical processing of stimuli depends, beside other factors, on the content and context of stimulation. A stimulus repetition represents a special case of stimulation, as the repeated stimulus contains the same information as its precursor. Its effects on cortical activity can be studied by event-related potentials (ERP) and event-related neuromagnetic fields (ERF). In the context of a uniform stimulation it seems to be plausible that the brain reacts less extensively on a repeated stimulation. Indeed, a decrease of the evoked activity can be observed under such conditions. This decrease has been characterized either on the neuronal level as an effect of refractoriness (Ritter et al., 1968) and on the behavioral level as a process of habituation, regarded as a primitive form of learning (Sokolov, 1977). Short-term habituation (STH) can be observed as the response decrease from stimuli to stimuli, by presenting sequences (or trains) of identical stimuli and averaging the cortical response for every stimulus position. Long-term habituation (LTH) describes the amplitude decrease over a longer time span, as minutes and hours.

In the context of permanently varying stimulation, a stimulus repetition might, however, represent a particular event and, in the auditory domain, it was assumed to evoke additional activity in form of a mismatch negativity (MMN). The MMN represents the earliest ERP component associated with a sound discrimination and deviance detection, first described by Näätänen et al. (1978). Normally the MMN is evoked by any discernible deviation in a sequence of repeated auditory stimuli and is thought to reflect an automatic pre-attentive change detection system (for more details on MMN see Näätänen and Winkler, 1999). The attempt to evoke a MMN by tone repetition in a sequence of varying tones represents the inversion of the traditional paradigm. The permanent variation of the standard tone is thought to produce an invariant feature of the environment, while the tone repetition is assumed to be a violation of this invariance.

Three studies were conducted in order to investigate whether a MMN can be elicited by the repetition of an auditory stimulus in the context of a permanently varying stimulation. Ritter et al. (1992) were not able to observe any MMN evoked by tone repetition, applying stimuli with a stimulus onset asynchrony (SOA) of 710 ms. Wolff and Schröger (2001) deduced from studies on tone omission and complex tone studies that a faster stimulation rate would be more favorable for the elicitation of a MMN by tone repetition. Indeed, the authors were successful to elicit a MMN by a repeated stimulus when stimuli were presented with a SOA of 160 ms. This positive finding was explained by the so-called temporal window of integration (TWI) (for more details see Näätänen and Winkler, 1999) which is assumed to reflect a sliding window of about 200 ms that integrates acoustic inputs from the same source or within a channel into a unitary percept. As the acoustic input within the TWI is treated as a unitary event whose constitutes belong together, Wolff and Schröger (2001) argued that a representation of the frequency change itself is established at short SOAs. A contrary explanation would be that tone repetition within the TWI leads to an increased duration of a coherent percept compared to non-repeated standard tones and the observed MMN is elicited by this increased duration. However, no clear-cut reason exists why the feature of a frequency change is represented in a sensory memory trace only when it occurs within this window and it is debatable why it should not be possible to evoke an MMN by tone repetition at a longer SOAs. Testing only a short SOA, the argumentation of Wolff and Schröger (2001) relies empirically only on the negative finding of Ritter et al. (1992). Indeed, in experiment 2 (condition 1) of Horvath et al. (2001) a “negative deflection whose characteristics were similar to that of the MMN component” (p. 141) was elicited by tone repetition at a SOA extending the TWI (500 ms).

The first aim of the current study was to clarify whether a MMN could be evoked by tone repetition at a SOA clearly extending the TWI. In course of this experiment with permanently varying auditory stimulation, possible deflections elicited by the tone repetition should be analyzed in their source configuration in order to investigate the nature of these deflections in detail. For this purpose magnetoencephalography (MEG) was used which is especially sensitive to tangential sources close to the head surface and which was, therefore, assumed to have a higher sensitivity than electroencephalography (EEG) for the MMN generator located in the superior temporal lobe.

The second aim of the study was to analyze the effects of stimulus repetition on the auditory evoked field component N100m, the neuromagnetic analogue of the electrophysiological N100. It was hypothesized that in the context of permanently varying auditory stimulation a stimulus repetition is reflected also in an amplitude reduction of the N100/N100m. This question was not explicitly addressed in the studies of Ritter et al., 1992, Horvath et al., 2001, Wolff and Schröger, 2001. Furthermore, I hypothesized that a possible decrease of N100m in the context of varying stimulation induced by tone repetition should have the same size as the decrease of the N100m in an STH experiment from the second to the third stimulus. Previous results on STH of the N100/N100m are, however, ambiguous: While some of the studies suggested that the decline of the N100 amplitude was complete after the second stimulus (EEG: Barry et al., 1992, Budd et al., 1998, Soininen et al., 1995; MEG: Lammertmann et al., 2001, Sörös et al., 2002), other studies revealed a more asymptotic amplitude (EEG: Fruhstorfer et al., 1970, Ritter et al., 1968, Woods and Elmasian, 1986; MEG: Sörös et al., 2001). In order to elucidate the N100/N100m decrease by stimulus repetition in more detail, a classical STH experiment with no tone variation was performed additionally with the same subject sample.

Taken together, effects of tone repetition on neuromagnetic auditory evoked fields (AEF) were investigated in the context of both permanently varying auditory stimulation and uniform stimulation.

Section snippets

Subjects

Sixteen young healthy subjects (6 males) with an average age of 25.3 years (range 21–28 years) took part in the study. With two exceptions all participants were familiar with the recording procedure, but none of the subjects had knowledge about the theoretical background of the study. After a thorough information all participants gave a written informed consent. The study was approved by the local ethics committee of the University of Jena.

Stimulation

AEF were obtained in two experimental conditions: in

Results

For 15 of 16 subjects AEF were successfully obtained. The data of one male subject were excluded prior to any off-line data analysis due to technical problems during the measurement and a low snr of the N100m. Because of the low snr the measurement was not repeated.

Discussion

The main findings can be summarized as follows. In the context of permanently varying acoustic stimuli a tone repetition elicited a small MMN in about 50% of the subjects. In this condition, the N100m dipole strength and latency was not affected significantly by tone repetition. In a traditional STH experiment a decrease in N100m dipole strength and decrease of its latency were observable only from the first to the second stimulus in the train. Afterwards on average no significant changes

Conclusion

It could be shown that an MMNm can be elicited by tone repetition in the context of varying stimulation even at SOAs extending the TWI. This finding supports the view of an automatic rule extraction within the auditory cortex, as proposed by Näätänen et al. (2001). The data on repeated stimulation with uniform tones reveal a dissociation between effects on N100m dipole moment and location, suggesting that the N100m consists of subcomponents with different recovery cycles or the N100m decrease

Acknowledgements

I would like to thank my colleagues Dr Ilonka Kreitschmann-Andermahr, Dr Marc Friederich and Dr Jens Haueisen for their helpful comments. I greatly appreciate the technical support for the MEG measurements by the Biomagnetic Center, Jena.

References (25)

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