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Clinical Trial
. 2013 Dec 9;8(12):e80899.
doi: 10.1371/journal.pone.0080899. eCollection 2013.

Modulatory Effects of Spectral Energy Contrasts on Lateral Inhibition in the Human Auditory Cortex: An MEG Study

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Free PMC article
Clinical Trial

Modulatory Effects of Spectral Energy Contrasts on Lateral Inhibition in the Human Auditory Cortex: An MEG Study

Alwina Stein et al. PLoS One. .
Free PMC article

Erratum in

  • PLoS One. 2014;9(7):e104051

Abstract

We investigated the modulation of lateral inhibition in the human auditory cortex by means of magnetoencephalography (MEG). In the first experiment, five acoustic masking stimuli (MS), consisting of noise passing through a digital notch filter which was centered at 1 kHz, were presented. The spectral energy contrasts of four MS were modified systematically by either amplifying or attenuating the edge-frequency bands around the notch (EFB) by 30 dB. Additionally, the width of EFB amplification/attenuation was varied (3/8 or 7/8 octave on each side of the notch). N1m and auditory steady state responses (ASSR), evoked by a test stimulus with a carrier frequency of 1 kHz, were evaluated. A consistent dependence of N1m responses upon the preceding MS was observed. The minimal N1m source strength was found in the narrowest amplified EFB condition, representing pronounced lateral inhibition of neurons with characteristic frequencies corresponding to the center frequency of the notch (NOTCH CF) in secondary auditory cortical areas. We tested in a second experiment whether an even narrower bandwidth of EFB amplification would result in further enhanced lateral inhibition of the NOTCH CF. Here three MS were presented, two of which were modified by amplifying 1/8 or 1/24 octave EFB width around the notch. We found that N1m responses were again significantly smaller in both amplified EFB conditions as compared to the NFN condition. To our knowledge, this is the first study demonstrating that the energy and width of the EFB around the notch modulate lateral inhibition in human secondary auditory cortical areas. Because it is assumed that chronic tinnitus is caused by a lack of lateral inhibition, these new insights could be used as a tool for further improvement of tinnitus treatments focusing on the lateral inhibition of neurons corresponding to the tinnitus frequency, such as the tailor-made notched music training.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Schematic representation of neural mechanisms as evoked by the masking stimuli (MS).
A. The lower part of the figure shows the frequency spectrum of the MS. The upper part is a highly simplified representation of neural activity in the auditory cortex as evoked by the MS. Neurons (excitatory = red, inhibitory = blue) are represented tonotopically. Transparent colors indicate reduced activation of inhibitory and excitatory neurons. Enlarged circles represent enhanced activation of neurons. B. Neurons with characteristic frequencies (CF) corresponding to the outer frequencies of the masking stimulus (OUT CF), the edge frequency bands (EFB) around the notch (EFB CF) and the frequencies within the notch (NOTCH CF) are further defined. A, B, C, D and E show the hypothesized modulation of neural mechanisms by MS with different spectral contrasts. The amount of lateral inhibition of neurons with NOTCH CF is hypothesized to be modulated in the following order (beginning with the greatest lateral inhibition of NOTCH CF): 3/8 oct +30 dB >7/8 oct +30 dB>NFN >3/8 oct −30 dB >7/8 oct −30 dB.
Figure 2
Figure 2. Schematic representation of a trial sequence.
A masking stimulus (MS) of 3 s was followed by a test stimulus (TS) of 1 s with an inter-stimulus interval of 0.5 s.
Figure 3
Figure 3. Auditory evoked magnetic field and contour map for the N1m response – experiment 1.
Example of the auditory evoked magnetic field and the corresponding contour map of a representative subject for N1m responses.
Figure 4
Figure 4. Grand averaged source waveforms, normalized source localizations and normalized N1m responses – experiment 1.
A. Grand averaged source waveforms for the N1m time window in the first experiment. N1m source strength is smallest in both amplified edge frequency band (EFB) conditions and greatest in both attenuated EFB conditions. The left panel shows the normalized source locations of both equivalent current dipoles (ECD) transformed to a standardized magnetic resonance imaging (MRI) brain. B. Mean normalized N1m values demonstrating the steady decrement of N1m responses with the smallest N1m source strength in the 3/8 octave amplified condition and the greatest in the 7/8 octave attenuated condition.
Figure 5
Figure 5. Auditory evoked magnetic field, contour map and normalized source localization for ASSR – experiment 1.
A. Example of the auditory evoked magnetic field and the corresponding contour map of a representative subject for auditory steady state responses (ASSR) in the first experiment. B. Normalized source locations of both equivalent current dipoles (ECD) transformed to a standardized magnetic resonance imaging (MRI) brain.
Figure 6
Figure 6. Auditory evoked magnetic field and contour map for the N1m response – experiment 2.
Example of the auditory evoked magnetic field and the corresponding contour map of a representative subject for N1m responses.
Figure 7
Figure 7. Grand averaged source waveforms and normalized N1m responses – experiment 2.
A. Grand averaged source waveforms for the N1m time window in the second experiment. N1m source strength is lower in both amplified edge frequency bands (EFB) conditions than in the notch-filtered noise (NFN) condition. N1m source strength in the narrower EFB amplification condition (1/24 oct +30 dB) seems to be greater than in the wider EFB amplification condition (1/8 oct +30 dB). The left panel shows the normalized source locations of both equivalent current dipoles (ECD) transformed to a standardized magnetic resonance imaging (MRI) brain. B. Mean normalized N1m values confirming the observed results in the grand averaged source waveforms.
Figure 8
Figure 8. Auditory magnetic evoked field, contour map, normalized source localization and interaction for ASSR – experiment 2.
A. Auditory evoked magnetic fields and the corresponding contour map of a representative subject for auditory steady state responses (ASSR) in the second experiment. B. Normalized source locations of both equivalent current dipoles (ECD) transformed to a normalized magnetic resonance imaging (MRI) brain. C. Interaction effect between the factors NFN-type and hemisphere for normalized ASSR source strengths. Error bars denote +/−1 standard error. Normalized ASSR source strengths are greater in both amplified conditions in the left hemisphere. NFN condition does not seem to differ between hemispheres.

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Publication types

Grant support

This research was supported by IZKF (CRA05) and Deutsche Forschungsgemeinschaft (PA 392/14-1). Hidehiko Okamoto was supported by the Japan Society for the Promotion of Science for Young Scientists (23689070). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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