Modulatory effect of inaudible high-frequency sounds on human acoustic perception

Neuroscience Letters 351 (2003) 191–195 www.elsevier.com/locate/neulet

Modulatory effect of inaudible high-frequency sounds on human acoustic perception Reiko Yagia, Emi Nishinaa,b,*, Manabu Hondac,d, Tsutomu Oohashie,f,g a

Department of Cyber Society and Culture, The Graduate University for Advanced Studies (SOKENDAI), Hayama, Kanagawa 240-0193, Japan b Human Interface Research and Development Section, National Institute of Multimedia Education, Chiba 261-0014, Japan c Laboratory of Cerebral Integration, National Institute for Physiological Sciences, Okazaki 444-8585, Japan d PRESTO, Japan Science and Technology Corporation, Kawaguchi 332-0012, Japan e Foundation for Advancement of International Science, Tokyo 164-0003, Japan f ATR Human Information Science Laboratories, Keihanna Science City, Kyoto 619-0288, Japan g Communications Research Laboratory, Koganei, Tokyo 184-8795, Japan Received 9 June 2003; received in revised form 16 July 2003; accepted 22 July 2003

Abstract We evaluated the effects of the intensity of an inaudible high-frequency component (HFC) of sound on human responses by employing a multi-parametric approach consisting of behavioral measurements of the comfortable listening level (CLL), psychological measurements of the subjective impression of sounds, and physiological measurements using electroencephalogram (EEG). Increasing the intensity of the inaudible HFC resulted in a significant increase in the CLL, the subjective impression of sounds, and the occipital alpha frequency component of the spontaneous EEG. These effects peaked with an increase of 6 dB in HFC intensity. The results of the present study suggest that the intensity of inaudible HFC non-linearly modulates human sound perception. q 2003 Elsevier Ireland Ltd. All rights reserved. Keywords: Hypersonic effect; Inaudible high-frequency component; Comfortable listening level; Electroencephalogram; Alpha frequency component; Sound perception

Using a multidisciplinary approach, quantifiably evaluating physiological, psychological, and behavioral responses, we found that sounds containing an inaudible high-frequency component (HFC) with non-stationary fluctuation evokes an increase in the regional cerebral blood flow in the brainstem and thalamus and in the occipital alpha frequency component of the spontaneous electroencephalogram (alpha-EEG) [8]. We also showed that the inclusion of an HFC makes the sound more comfortable for listening [8] and introduces a specific behavior; the subjects spontaneously adjust the comfortable listening level (CLL) of the sound to a greater magnitude using various sound sources [7]. These effects were confirmed using various sound sources [7]. We term these phenomena collectively as the ‘hypersonic effect’. The combined presentation of an HFC and an audible low-frequency component (LFC), not an HFC alone, evokes the hypersonic effect [8], thus, the *

Corresponding author. Tel.: þ 81-43-298-3222; fax: þ81-43-298-3482. E-mail address: [email protected] (E. Nishina).

effect of an HFC appears to be primarily modulatory. In the present study, to investigate the neuronal mechanisms underlying the hypersonic effect, we examined the doseresponse relation between the intensity of an HFC and human sound perception. For this purpose, we employed multi-parametric measurements of behavioral, psychological, and physiological responses to increases in the intensity of an inaudible HFC in otherwise identical sounds. Traditional gamelan music ‘Gambang Kuta’ of Bali Island, Indonesia, recorded on the Authentic Signal Disc (ARHS-9002; Action Research Co., Ltd., Tokyo, Japan), was used as the auditory stimuli for all the experiments. This signal disc contained the HFC and LFC, into which the original sound source was divided using programmable high-pass and low-pass filters (FV-661; NF Electronic Instruments, Yokohama, Japan) with a crossover frequency of 22 kHz and a cut-off attenuation of 80 dB/octave, in separate channels. The Authentic Hypersonic Audio System (Action Research Co., Ltd.) consisting of a bi-channel sound

0304-3940/03/$ - see front matter q 2003 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/S0304-3940(03)00884-X

192

R. Yagi et al. / Neuroscience Letters 351 (2003) 191–195

presentation system [8] was used to present the stimuli. Thus the HFC and LFC of the sound source were independently amplified and presented. Detailed information of the signal disc and the sound presentation system has been described previously [15]. The intensity of the HFC was controlled using a volume controller of the pre-amplifier for the HFC. Three experimental conditions in which the intensity of the HFC was set at three different levels were prepared: 0, þ 6, and þ 12 dB (Fig. 1). Under the 0 dB condition, the HFC of the original stimuli was presented without enhancement. Under the þ 6 or þ 12 dB conditions, the intensity of the HFC was increased to each level (i.e. approximately two or four times in amplitude of that under 0 dB condition). Note that the intensity of the LFC was identical across the three conditions. The A-weighted sound pressure level (LA eq) of the presented LFC was measured using an integrated sound level meter (LA-5111; ONO SOKKI, Yokohama, Japan), which measures the LA eq of the sounds below 22 kHz. The three conditions were confirmed to be equal within an error of less than 0.1 dB. The subjects sat comfortably on a chair throughout the experiment. The distance from the surface of the speaker to the subjects’ ears was approximately 2 m. The room temperature, furniture, and especially the visual environment were organized so as to maintain the comfort of the subjects. In the behavioral experiment, the CLL was used as a measure of perception of subtle differences in sound quality that may not be consciously recognizable or otherwise easily expressed by the subjects [5]. Previous studies have shown that the CLL depends on several factors, including the degree to which the sounds appear to the subjects as being ‘live’ or recorded, the physical structure of the sound signal [4], and the listeners’ feelings of pleasantness and unpleasantness [2,12]. Fifteen healthy volunteers (six males and nine females, mean age ¼ 40.5 ^ 10.9 years) with normal hearing acuity participated in this experiment. They

Fig. 1. Mean power spectra of the sounds reproduced by the bi-channel sound presentation system under different conditions. The power spectra was calculated from the signal recorded at the subject’s head position using a B&K 4135 microphone (Bru¨ el & Kjær, Nærum, Denmark). Using a volume controller of the pre-amplifier, only the inaudible high-frequency component above 22 kHz was increased by þ 6 (orange) or þ 12 dB (green) relative to the original sound (0 dB: blue).

were requested to have at least 7 h of sleep the night before the experiment and to awaken at least 2 h before the experiment to ensure that they were sufficiently alert. One experimental session consisted of six trials, each of which was a 60-s presentation of the same sound material. Throughout a single session, the same stimulus (i.e. 0, þ 6, or þ 12 dB) was presented. In the first two trials, the subjects listened to the sound at a fixed volume adjusted to 75.0 dB (LA eq) at the listening position. Then, during the following three trials, the subjects were requested to freely adjust the volume to what they considered to be a comfortable level using a remote control with an up-down switch that controlled the motorized fader (PGFM3000; Penny & Giles, Gwent, United Kingdom) inserted between the Super Audio Compact Disc player and the pre-amplifier. No visual or tactile information of the volume was given to the subjects when they adjusted the volume. Then, during the final trial, each subject listened to the sound fixed at the volume level that they had determined at the end of the previous trial. The listening level was measured as LA eq during each trial with the integrated sound level meter, and the level measured in the final trial was considered to be the CLL. Each subject performed three sessions of the three different conditions, conducted in a counter balanced order across subjects, who were blind to the conditions of the sessions. As the trials progressed, the listening level of the conditions with enhanced HFC became higher than the original sound (0 dB condition; Fig. 2a). The mean CLLs in the final trial of each condition are shown in Fig. 2b. Repeated measure analysis of variance (RM-ANOVA) revealed the main effect of the experimental condition (Fð2; 28Þ ¼ 3:852, P , 0:05). There was a significant difference in CLL between the 0 dB condition and either the þ 6 or þ 12 dB conditions (0 versus þ 6 dB: t ¼ 2:50, P , 0:05; 0 versus þ 12 dB: t ¼ 2:32, P , 0:05). The CLLs of the þ 6 and þ 12 dB conditions were not significantly different. In the psychological experiment, the subjective impression of the sound was evaluated via questionnaires. Twelve subjects (five male and seven female, mean age ¼ 40.8 ^ 12.0 years), all of whom participated in the behavioral experiment, were studied. One session consisted of a pair of trials of different conditions with an inter-trial interval of 10 s. Each trial consisted of two presentations of the 60-s sound stimuli used in the behavioral experiment. The listening level of each condition for each subject was set at the CLL determined by the subject in the behavioral experiment. Six sessions with different combinations and orders of the three experimental conditions were performed for each subject. The order of the sessions was counter balanced across the subjects who were blind to the conditions of the sessions. The subjects filled out a questionnaire to rate the sound quality in terms of 20 elements, each expressed in a pair of contrasting Japanese words (e.g. soft versus hard). Each element of each condition was graded on a scale of 1– 5. The scores were

R. Yagi et al. / Neuroscience Letters 351 (2003) 191–195

193

stimuli used in the behavioral and psychological experiments. Two sessions were performed with an inter-session interval of several minutes. The conditions in the second session were in the reverse order of the first one. The EEGs were recorded from 12 scalp sites (Fp1, Fp2, F7, Fz, F8, C3, C4, T5, Pz, T6, O1, and O2) according to the International 10 – 20 System using linked earlobe electrodes as the reference with a filter setting of 1– 60 Hz (2 3 dB). A telemetric system was used to minimize restriction of the movements of the subjects. The power spectrum of the EEG at each electrode was calculated by Fast Fourier Transform analysis for every 2-s epoch with an overlap of 1 s. Then the square root of the power level in a frequency range of alpha band (8.0 – 13.0 Hz) at each electrode position was calculated as the alpha-EEG. Considering the delay of the hypersonic effect [8], the alpha-EEGs at each electrode position were averaged during latter half (i.e. 90 s) of the sound presentation. To remove relatively large variability of the alpha-EEG across subjects, the values were normalized with respect to the mean value across all the conditions and electrode positions for each subject, and colored contour line maps were constructed (Fig. 3a) [3]. For a statistical evaluation, the occipital alpha-EEG was calculated by averaging the alpha-EEGs at T5, Pz, T6, O1, and O2 to avoid contamination from artifacts arising from eye move-

Fig. 2. Listening levels under each condition in the behavioral experiment. (a) Time course of the listening level. During the Adjust 1, 2, and 3 trials, the subjects adjusted the volume to what they considered to be a comfortable level. The listening level was measured as the equivalent continuous A-weighted sound pressure level (LA eq). (b) Mean and standard error of the CLL under each condition. The volume was fixed at the level determined by each subject at the end of the Adjust 3 trial under each condition.

statistically evaluated using Scheffe´ ’s paired comparison (Table 1) [11]. A significant difference in sound quality was detected in 14 out of 20 elements across experimental conditions. Overall, the subjects felt that þ 6 dB condition was the most comfortable among the three conditions. In the physiological experiment, ten subjects (four male and six female, mean age ¼ 39.2 ^ 11.9 years), all of whom participated in the behavioral experiment, were studied. One session consisted of three trials, one for each condition, with 3-min inter-trial intervals. The listening level of each condition for each subject was set at the CLLs determined by the subject in the behavioral experiment. The order of the conditions was counter balanced across the subjects who were blind to the conditions of the sessions. Each trial consisted of the presentation of the 180-s sound

Fig. 3. Normalized alpha-EEG potentials under each condition in the physiological experiment. (a) Overall mean topographical maps of the power of the alpha frequency component under each condition. Darker red indicates higher alpha-EEG potential. (b) Mean and standard error of the occipital alpha-EEG under each condition.

194

R. Yagi et al. / Neuroscience Letters 351 (2003) 191–195

Table 1 Statistical evaluation of the subjective impression of sounds Element for evaluationa

Rich in mood – poor in mood Rich in nuance – lacking in nuance Thick – thin Natural – artificial Realistic – unrealistic Rich in information – lacking in information Finely textured – roughly textured Deep – shallow Lower tone dominant – higher tone dominant Moist – dry Like – dislike Not tiring – tiring Balanced instruments – unbalanced instruments Resonant type – percussive type Wide – narrow Comfortable to ears – uncomfortable to ears Alive – calm Light – heavy Soft – hard Relaxing – tensive

Paired comparisons between conditions (P)b

Main effect F(2,35)

P

þ 6 versus 0 dB

þ 12 versus 0 dB

þ6 versus þ12 dB

16.53 11.83 9.81 7.69 7.38 6.94 6.55 6.31 6.01 5.86 5.73 5.47 4.28 3.29 2.78 2.24 1.35 1.03 1.02 0.91

** ** ** ** ** ** ** ** ** ** ** ** * * n.s. n.s. n.s. n.s. n.s. n.s.

** ** ** ** ** ** ** ** ** ** ** ** * * – – – – – –

n.s. * n.s. n.s. * n.s. n.s. * n.s. n.s. n.s. n.s. n.s. n.s. – – – – – –

** n.s. * n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. ** n.s. n.s. – – – – – –

*P , 0.05; **P , 0.01; n.s. ¼ not significant. Approximate English equivalents for pairs of Japanese words used for psychological experiment. The subjects rated sound quality on a scale of 5 (left) to 1 (right). b P indicates the significance level by which the former condition showed higher score than the latter for each evaluation. When the main effect was not significant, paired comparisons were not performed. a

ment (Fig. 3b). The alpha-EEG was enhanced during the þ 6 dB condition compared to the other conditions. RMANOVA revealed a significant main effect of the experimental conditions (Fð2; 30Þ ¼ 4:06, P , 0:05). The occipital alpha-EEG during the þ 6 dB condition was significantly greater than that during the 0 dB condition (t ¼ 2:75, P , 0:05). Although the difference between the þ 6 and þ 12 dB conditions was not statistically significantly different (t ¼ 1:69, P ¼ 0:11), the mean occipital alpha-EEG tended to decrease under the þ 12 dB condition. On the other hand, the alpha-EEG did not show any correlation with the listening level (r ¼ 0:062, P ¼ 0:67), which suggests the difference in the alpha-EEG cannot be explained by mere the difference in averaged listening level across conditions. Taken together, the results of the present study demonstrate that an enhanced HFC increased the CLL and improved the subjective impression of the sound in association with an increase in the alpha-EEG. These effects were most prominent with an increase of þ 6 dB in the HFC, plateauing or decreasing again with a further increase in the HFC. These results suggest that the inaudible HFC has a modulatory effect on human sound perception and that such an effect may not linearly increase as the intensity of the HFC increases, but has some optimum point. We have previously shown that the amplitude of the occipital alpha-EEG is positively correlated with the regional cerebral blood flow in deep-lying brain structures

including thalamus [8,10]. This area contains distinct neuronal groups that are the major source of the monoaminergic projections to various parts of the brain [9]. These fibers lie in the medial forebrain bundle, which is considered to be intimately connected with registering pleasurable sensations [13]. These previous results led us to propose the two-dimensional sound perception model [7,8], that is, that sound frequencies in the audible range function as a message carrier, and frequencies above the audible range, together with those in the audible range, function as a modulator of sound perception through the brain systems including the reward-generating system [1,6]. In the present study, an increase in the intensity of the HFC was associated with an intensification of the pleasurable aspect of the sound perception and evoked a behavioral response of increasing the intensity of the stimulus, thus we envisage the participation of the same modulatory system. Indeed, the non-linear dose-response relation between the intensity of the HFC and human response is consistent with the nonlinear characteristics of the reward-generating system [14]. The present findings further support the two-dimensional sound perception model.

Acknowledgements We thank Dr Toshie Nakamura of the Graduate School of Human Sciences, Osaka University, for her thoughtful

R. Yagi et al. / Neuroscience Letters 351 (2003) 191–195

advice; Dr Yoshio Yamasaki of Waseda University and Prof. Masami Toyoshima of Yokkaichi University for their support in system development; Dr Tadao Maekawa of NTT Cyber Solutions Laboratories, Dr Satoshi Nakamura of Japan Science and Technology Corporation, Dr Masako Morimoto of Jumonji Gakuen Women’s University, Dr Norie Kawai and Dr Osamu Ueno of Foundation for Advancement of International Science for their technical support. This work was supported in part by the Ministry of Education, Culture, Sports, Science, and Technology of Japan through a Grant-In-Aid for Scientific Research (B) 13450173 for E.N. and by the Nissan Science Foundation for T.O.

References [1] S.J. Cooper, Interactions between endogenous opioids and dopamine: implication for reward and aversion, in: P. Willner, J. Scheel-Kruger (Eds.), ‘The Mesolimbic Dopamine System’. Motivation to Action, Wiley & Sons, New York, 1991, pp. 331 –366. [2] S. Cullari, O. Semanchick, Music preferences and perception of loudness, Percept. Mot. Skills 68 (1989) 186. [3] F.H. Duffy, J.L. Burchfiel, C.T. Lombroso, Brain electrical activity mapping (BEAM): a method for extending the clinical utility of EEG and evoked potential data, Ann. Neurol. 5 (1979) 309–321. [4] S. Iwamiya, T. Suzuki, Optimum listening level of music, Ann. Psysiol. Anthrop. 7 (1988) 175– 182. [5] S. Namba, S. Kuwano, Method of Psychological Measurement for Hearing Research (in Japanese), Colona Publishing, Tokyo, 1998, pp. 166–168.

195

[6] J. Olds, P. Milner, Positive reinforcement produced by electrical stimulation of septal area and other regions of the rat brain, J. Comp. Physiol. Psychol. 47 (1954) 419 –427. [7] T. Oohashi, E. Nishina, M. Honda, Multidisciplinary study on the hypersonic effect, in: H. Shibasaki, H. Fukuyama, T. Nagamine, T. Mima (Eds.), Inter-areal Coupling of Human Brain Function, Elsevier Science, Amsterdam, 2001, pp. 27–42. [8] T. Oohashi, E. Nishina, M. Honda, Y. Yonekura, Y. Fuwamoto, N. Kawai, T. Maekawa, S. Nakamura, H. Fukuyama, H. Shibasaki, Inaudible high-frequency sounds affect brain activity: hypersonic effect, J. Neurophysiol. 83 (2000) 3548–3558. [9] L.W. Role, J.P. Kelly, The brain stem: cranial nerve nuclei and the monoaminergic systems, in: E.R. Kandel, J.H. Schwartz, T.M. Jessell (Eds.), Principle of Neural Science, Appleton & Lange, Connecticut, 1991, pp. 869–883. [10] N. Sadato, S. Nakamura, T. Oohashi, E. Nishina, Y. Fuwamoto, A. Waki, Y. Yonekura, Neural networks for generation and suppression of alpha rhythm: a PET study, NeuroReport 9 (1998) 893– 897. [11] H. Scheffe´ , An analysis of variance for paired comparisons, J. Am. Stat. Ass. 47 (1952) 381–400. [12] D.S. Smith, Preferences for differentiated frequency loudness levels in older adult music listening, J. Music-Ther. 26 (1989) 18–29. [13] J.G. Thompson, The Psychobiology of Emotions, Plenum Press, New York, 1988, pp. 24–42. [14] R.A. Wise, P. Bauco, W.A. Carlezon Jr, W. Trojniar, Self-stimulation and drug reward mechanisms, Ann. N. Y. Acad. Sci. 654 (1992) 192–198. [15] R. Yagi, E. Nishina, N. Kawai, M. Honda, T. Maekawa, S. Nakamura, M. Morimoto, K. Sanada, M. Toyoshima, T. Oohashi, Auditory Display for Deep Brain Activation: Hypersonic Effect, The 8th International Conference on Auditory Display, Kyoto, 2002, pp. 248–253.