On the Origin of the 1,000 Hz Peak in the Spectrum of the Human Tympanic Electrical Noise

Abstract

The spectral analysis of the spontaneous activity recorded with an electrode positioned near the round window of the guinea pig cochlea shows a broad energy peak between 800 and 1,000 Hz. This spontaneous electric activity is called round window noise or ensemble background activity. In guinea pigs, the proposed origin of this peak is the random sum of the extracellular field potentials generated by action potentials of auditory nerve neurons. In this study, we used a non-invasive method to record the tympanic electric noise (TEN) in humans by means of a tympanic wick electrode. We recorded a total of 24 volunteers, under silent conditions or in response to stimuli of different modalities, including auditory, vestibular, and motor activity. Our results show a reliable peak of spontaneous activity at ~1,000 Hz in all studied subjects. In addition, we found stimulus-driven responses with broad-band noise that in most subjects produced an increase in the magnitude of the energy band around 1,000 Hz (between 650 and 1,200 Hz). Our results with the vestibular stimulation were not conclusive, as we found responses with all caloric stimuli, including 37°C. No responses were observed with motor tasks, like eye movements or blinking. We demonstrate the feasibility of recording neural activity from the electric noise of the tympanic membrane with a non-invasive method. From our results, we suggest that the 1,000 Hz component of the TEN has a mixed origin including peripheral and central auditory pathways. This research opens up the possibility of future clinical non-invasive techniques for the functional study of auditory and vestibular nerves in humans.

Keywords: auditory nerve; electrocochleography; round window noise; spontaneous activity; tympanic membrane; vestibular nerve.

Figure 1

Power spectrum of the tympanic electric noise. Each colored curve represents one different subject. Note the presence of a broad peak in all subjects around 1,000 Hz. The missing points in the curves were eliminated by the denoise procedure (described in the Methods section).

Figure 2

Time spectrum of the tympanic electric noise in humans. This spectrogram shows the stability of the 1,000 Hz peak throughout a complete session of tympanic electric noise recording (360 s) in one subject. Notice that, although the spectral peak is centered around 1,000 Hz, at the single epoch level (each dot in the time spectrum), varies between 800 Hz and 1,200 Hz. This figure shows data before the denoise procedure. The subject corresponds to the volunteer with the largest peak at 1,000 Hz in Figure 1.

Figure 3

Tympanic electric noise ECG-like and EMG controls. (A) Comparison between TEN and ECG-like spectrums. The blue line shows the averaged spectrogram of a 360 s recording from an ECG-like signal with wrist electrodes, while the red line shows the spectrum of the TEN signal in the same volunteer. To compare the wrist and eardrum noise signal, the y-axis is shown in arbitrary units measured in dB of attenuation. The frequency components of the ECG-like signal are probably observed in the low frequency band (<100 Hz) of the corresponding power spectrum. (B) TEN spectrum with (red) and without (black) masseter muscle activation. Volunteers activated their masseter muscles through isometric contraction, with mouth closed during 1 min. Note that the muscle activation produces a power increase in the frequency band <800 Hz, but not in the 1,000 Hz peak, probably related to EMG activity.

Figure 4

Increase of the TEN 1,000 Hz peak amplitude during auditory stimulation with broad-band noise in the majority of the subjects (n = 9). This graph shows the effect (in dB) of broad-band noise stimulation on the nine subjects with an increase in the amplitude of the TEN 1,000 Hz peak (measured as the integral value between 650 and 1,200 Hz) [One way ANOVA, F₍₂₎ = 241.420, p < 0.001; Tukey post-hoc, p < 0.05 in the three pairwise comparisons]. In addition to the amplitude increase of the TEN 1,000 Hz peak observed in these nine subjects, in two cases we found an amplitude decrease with broad-band noise stimulation.

Figure 5

Time and power spectrums of the tympanic electric noise with broad-band noise stimulation. (A) Time spectrum, the filtered broad-band noise (>4 kHz) increases the TEN 1,000 Hz peak at 72 and 82 dB. Notice the presence of a cochlear microphonic component above 2 kHz with broad-band noise stimulation. (B) Spectrum of the averaged signals in silence (baseline) and with 72 and 82 dB SPL. This figure shows data before the denoise procedure.

Figure 6

Increase of the TEN 1,000 Hz peak during vestibular caloric stimulation at 26°C (blue), 49°C (red), and 37°C (green). This figure show box-plots of TEN 1,000 Hz peak amplitudes for baseline and caloric stimulation at 26 and 49°C in eight volunteers and at 37°C for three subjects, showing the effect in dB of change (measured as the integral value between 650 and 1,200 Hz). Note that the amplitude of the 1,000 Hz peak of TEN does not return to base levels after warm stimulation at 49°C. [Cold air: Kruskal–Wallis analysis, H₍₂₎ = 6.038, p = 0.037, Dunn post-hoc test p < 0.05; warm air: Kruskal-Wallis analysis, H₍₂₎ = 9.420, p = 0.009]. Stimulation at 37°C also produced an increase of the 1,000 Hz peak of the TEN (b, baseline and p, recovery period).

Figure 7

Time and power spectrums of the tympanic electric noise with cold air stimulation at 26°C. (A) Notice the presence of low frequency artifacts at the beginning and at the end of the caloric stimulation (around 60 and 180 s), while there is a progressive increase of the 1,000 Hz peak during vestibular stimulation (between 60 and 180 s). (B) Spectrum of the averaged signals during baseline period, during the first and second minutes of caloric stimulation and after cold stimulation. Notice that the largest 1,000 Hz peak was obtained in the second minute of cold stimulation. This figure shows data before the denoise procedure.