International Journal of Audiology 2013; 52: 139–143
Clinical Note
Auditory steady state response in sound field H. Hernández-Pérez & A. Torres-Fortuny Speech and Hearing Sciences Department, Cuban Neuroscience Center, Habana, Cuba
Abstract Objective: Physiological and behavioral responses were compared in normal-hearing subjects via analyses of the auditory steady-state response (ASSR) and conventional audiometry under sound field conditions. Design: The auditory stimuli, presented through a loudspeaker, consisted of four carrier tones (500, 1000, 2000, and 4000 Hz), presented singly for behavioral testing but combined (multiple frequency technique), to estimate thresholds using the ASSR. Study sample: Twenty normal-hearing adults were examined. Results: The average differences between the physiological and behavioral thresholds were between 17 and 22 dB HL. The Spearman rank correlation between ASSR and behavioral thresholds was significant for all frequencies (p ⬍ 0.05). Significant differences were found in the ASSR amplitude among frequencies, and strong correlations between the ASSR amplitude and the stimulus level (p ⬍ 0.05). Conclusions: The ASSR in sound field testing was found to yield hearing threshold estimates deemed to be reasonably well correlated with behaviorally assessed thresholds.
Key Words: Auditory steady state response; electric response audiometry; sound field; normal hearing
The auditory steady state response (ASSR) has received much attention for purposes of electric response audiometry (ERA) (Tlumak et al, 2007). Among several ways in which the responses can be stimulated and measured, one of the most basic is to use single or multiple continuous tones amplitude modulated (AM) at rates between 75–110 Hz, and thus an alternative to objective frequency-specific audiometry using more traditional transient stimulus-response methods. To evoke the ASSR, the stimuli can be conducted by air (headphones, insert earphones or loudspeaker), bone (bone vibrator), or electrically (in cochlear implant subjects). ASSRs generated using headphones have been extensively studied and provide reasonably reliable estimates of hearing thresholds: e.g. in hearing-impaired subjects to within 12–15 dB HL of the behavioral thresholds (Lins & Picton, 1995; Rance et al, 1995; Lins et al, 1996; Pérez-Abalo et al, 2001; Dimitrijevic et al, 2001; Rance & Briggs 2002; Rance & Tomlin, 2006; Tlumak et al, 2006). ASSR to single or multiple frequency stimuli can also be presented through a bone transducer positioned on one of the mastoids. The thresholds, obtained using this technique are approximately 10 dB above the behavioral thresholds (Lins et al, 1996; Cone-Wesson et al, 2002; Small & Stapells, 2005, 2006). This technique may have the advantage of distinguishing between sensory-neural, conductive, and mixed loss (Brooke et al, 2009), but has the disadvantage of generating substantial electrical artifact induced at
the modulation frequency by the proximity of the vibrator to the recording electrodes (Dimitrijevic et al, 2002; Gorga et al, 2004; Picton & John, 2004; Small & Stapells, 2004). ASSR ERA has yet to come into common use in the evaluation of amplification gain of hearing devices or other habilitative/ rehabilitative applications in the pediatric clinical population (Hatzopoulos et al, 2010). Furthermore, eliciting an ASSR using sound field stimulation has received little attention in the research literature. This form of presentation may reduce stimulus artifactual component that might be realized by less proximity of the transducer to the recording electrodes and wiring (re: the headphone or bone vibrator). Picton et al, 1998; Stroebel et al, 2007, and Damarla, 2007 thus have proposed recording the ASSR in the sound field for evaluating the amplification gain in hearingaid subjects. Similarly, Swanepoel, 2004 and Attias et al, 2006 have used this approach to estimate hearing thresholds in young cochlear implant candidates. Still, there remain inadequate results in the literature to permit characterizing the results of ASSR testing under sound field stimulation, starting with normal-hearing subjects. Therefore, the purpose of this study was to compare behavioral and physiological thresholds estimates by way of analysis of ASSR amplitudes to multiple amplitude modulated tones in normal-hearing subjects using sound field presentation.
Correspondence: Alejandro Torres-Fortuny, Ave. 25 #15202 and 158, Cubanacan, Playa, Area Code 11600, Habana, P.O.B 6412 /6414, Cuba. E-mail:
[email protected] (Received 25 August 2011; accepted 26 August 2012) ISSN 1499-2027 print/ISSN 1708-8186 online © 2013 British Society of Audiology, International Society of Audiology, and Nordic Audiological Society DOI: 10.3109/14992027.2012.727103
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Abbreviations ASSR ERA
Auditory steady state response Electric response audiometry
Methods Subjects Twenty normal-hearing adults (nine of which were female) took part in this study with ages ranging from 24–30 years (mean of 27 ⫾ 3). An informed consent was obtained from all the subjects, who were volunteers recruited from the staff of the Cuban Neuroscience Center.
Auditory stimuli The stimuli were delivered by the (AUDIX system, NEURONIC S.A., Havana; see http://www.courses.audiospeech.ubc.ca/ haplab/ASSR.html for more information). The system’s output was directly connected to the loudspeaker (B&W Loudspeakers, Ltd; DM 601 S3): output of 100 w / 8 Ω, frequency response of 60–22 000 Hz ⫾ 3 dB on reference axis and harmonic distortions for the 2nd & 3rd harmonics ⬍ 1% 88–20 000 Hz (90 dB SPL, 1 m). The stimuli consisted of a combination of four sinusoidal carrier tones of 500, 1000, 2000, and 4000 Hz modulated in amplitude (95% depth) at the following rates: 104.2, 107.8, 111.4, and 115 Hz respectively. They were presented binaurally with the subject facing a single loudspeaker. Each tone was added to one of the other to create the multiple frequency stimuli. The ISO 389-7 (1998) standard provides reference sound field hearing thresholds for calibrations purposes where the sound source is at frontal position (0° azimuth). Each carrier frequency was adjusted in intensity according to the audibility differences among the individual tones. The stimuli were calibrated in dB HL, and the loudspeaker reproduced it accurately.
Recording Electrode discs of Ag/AgCl were fixed with electrolytic paste at Cz (positive), 2.5 cm below inion (negative), and Fpz (ground). Impedance values were kept below 5 kOhms at 10 Hz. The bioelectric activity was amplified with a resolution of 16 bit (0.012 μV) and analog filtered between 10 and 300 Hz (high-pass 1st order: Fl ⫽ 10 Hz (⫺3 dB, ⫺6 dB/octave) and low-pass, Fh ⫽ 300 Hz (⫺3 dB, ⫺18 dB/octave; Butterworth response characteristics). The responses were averaged between 7 and 24 epochs of 8192 samples (digitized with a sampling period of 1.08 msec) for recording times of 5 to 15 minutes, respectively. The subjects reposed comfortably on a bed in a sound treated room (3 ⫻ 3 m). The test booth interior was dimly lit, and the subjects were encouraged to relax and to fall asleep in order to reduce the residual noise level (RNL). In any event, the subjects were requested to make no movement. The subjects could be observed during recordings through the room’s window. When a subject would move his/her head on falling asleep, the recording was stopped and the head was repositioned. The loudspeaker was situated 2 m from the subject’s head (distance recommended by The Guidelines for Sound Field Audiometry in Clinical Audiological Applications, (British Society of Audiology, 2007) (thus more than three wavelengths at 500 Hz and
above) at 0° azimuth at all times. The height of the loudspeaker was adjusted so as to be elevated 0.4 m above the bed. The measurement of acoustic noise (environment noise) was made with a Brüel & Kjaer sound level meter (Investigator 2250 with microphone type 4189) inside the room. The microphone was aligned with the position of midline of the subjects’ head. The value of 54 dB SPL (dB SPL) corresponds to the global environment noise (total frequency contribution). The level per cycle of the ambient noise measured in the vicinity of the test frequencies 500, 1000, 2000, and 4000 Hz as approximately 31, 30, 30, and 31 dB SPL respectively over a measured bandwidth of 250 to 8000 Hz.
Experimental design The aim was to try to follow a protocol to make results directly applicable in routine clinical procedures. In all cases behavioral thresholds were determined using the psycho-acoustic technique of ascending and descending limits (10 dB up and 5 dB down, re: Carhart & Jerger, 1959) with sound field presentation, as above for behavioral testing, thresholds were measured using the AM stimuli presented singly. The physiological threshold estimates were determined by the presence or absence of recognizable steady-state responses recorded under multi-tone stimulation. For suprathreshold levels, the ASSR was always averaged with a minimum of 7 epochs. The stopping criterion was a residual noise level lower than 0.002 μV through a maximum number of 24 sweeps. The multiple frequency stimuli were presented in a series of decreasing intensities (steps of 10 dB HL; from 60 dB HL until reaching the individuals’ physiological thresholds). Also analysed were the ASSR amplitudes obtained at suprathresholds HLs per frequency.
Statistical methods for response detection The statistical test used for assessing the presence of a significance response is based on a variant of the multivariate Hotelling T2 statistic (see Valdés et al, 1997). The test consists in a multivariate comparison (using vectors formed by the real and imaginary part) of the Fourier components for each modulation frequency (Fp) vs. the average of Fourier components for adjacent (no modulation) frequencies (MeanFn). The latter is computed from 60 frequencies above and below the corresponding modulation frequency and is considered an estimate of noise level (120 frequencies in total). Then, the statistic for measuring the deviation of the signal from the noise level at a given frequency component is: T2H ⫽ N(Fp ⫺ MeanFn)′∗(Fp ⫺ MeanFn)/VarFn The apostrophe represents transposition of the vectors, and VarFn represents an estimate of the variance of the noise across all 120 adjacent frequencies. This statistic is proportional to an F statistic which follows a Fisher distribution with 2 and 118 degrees of freedom (Mardia et al, 1979), and from which 95% confidence limits can be obtained. These limits allow us to establish which responses (in each modulation frequency) are significantly different from the noise level.
Statistical design The statistical evaluations were carried out using Statistic 8.0. The mean and standard deviations of the physiological and behavioral
ASSR in sound field thresholds and the differences between them were assessed. Also the mean and standard deviations of the ASSR amplitude values were calculated. Spearman correlations between physiological and behavioral thresholds and Pearson correlations between and the ASSR amplitude values and stimulation intensities were calculated using the null hypothesis of no correlation between curves (p ⬍ 0.05). A one-way ANOVA analysis was used to explore if ASSR amplitude were different between frequencies (p ⬍ 0.05).
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Table 2. Distribution of individual ASSR thresholds. Thresholds (dB HL) 60 50 40 30 20
500 Hz
1000 Hz
2000 Hz
4000 Hz
7 13
1 6 9 4
1 5 11 3
1 6 10 2 1
Results and Discussion Physiological and behavioral thresholds in normal subjects We obtain physiological thresholds in the subjects who comprise the sample. The physiological thresholds were between 17 and 22 dB above the behavioral thresholds (see Table 1). The differences between thresholds reported in normal-hearing subjects using earphones (Lins et al, 1996; Pérez-Abalo et al, 2001; Herdman & Stapells, 2003) and bone stimulation (Small & Stapells, 2004, 2005) are between 10–15 dB. However our findings can only be directly compared with one previous study. Picton et al, 1998 studied 10 normal-hearing subjects in similar free sound-field recording conditions and obtained differences between 18 and 26 dB. Since Picton et al report thresholds in dB SPL, we use the reference free field thresholds for equipment calibration ISO 389-7 (1998), to convert their thresholds into dB HL thresholds. The reference values were added to each difference between thresholds reported by Picton et al. With these transformations, we infer differences in the values of Picton et al between 19 and 22 dB; differences similar to those we have found. However our thresholds for normal-hearing subjects under free sound-field conditions are higher than those reported by Picton et al. The global environment noise reported here could be the cause of this discrepancy. Our ambient noise levels could elevate the behavioral and physiological thresholds. However, in this case, the ambient noise level should affect both thresholds equally, thus maintaining an accurate estimation of the differences between thresholds. This may be why both studies report similar differences between physiological and behavioral thresholds. Therefore, we believe that in normal-hearing subjects under free field sound conditions, the differences between thresholds are higher than those reported for direct air or bone stimulation. Nevertheless, this hypothesis should be tested with new experiments. A significant Spearman correlation between thresholds was found. The correlation between the thresholds in normal-hearing subjects was significant for all frequencies: 500 Hz (r ⫽ 0.67; p ⬍ 0.001); 1000 Hz (r ⫽ 0.77; p ⬍ 0.001); 2000 Hz (r ⫽ 0.73; p ⬍ 0.001); 4000 Hz (r ⫽ 0.68; p ⬍ 0.001), and total correlation (r ⫽ 0.70; p ⬍ 0.001). The Pearson correlations between thresholds reported in the literature using ASSR with multiple frequencies under air conditions were between 0.7 and 0.91 (Picton et al, 2003). Our r-values (between 0.67 and 0.77) are consistent with this and indicate that ASSRs are Table 1. Physiological and behavioral thresholds using multiple frequency technique. Thresholds (dB HL)
500 Hz
1000 Hz
2000 Hz
4000 Hz
Behavioral Physiological Difference
22 ⫾ 6 43 ⫾ 5 21 ⫾ 7
22 ⫾ 6 43 ⫾ 8 21 ⫾ 12
25 ⫾ 6 42 ⫾ 8 17 ⫾ 11
20 ⫾ 8 42 ⫾ 9 22 ⫾ 12
Mean ⫾ SD.
strongly correlated with the behavioral thresholds. Our findings confirm that the ASSR using multiple frequencies under free field conditions is a useful means of obtaining an accurate estimate of hearing thresholds. Our results show that it is feasible to obtain ASSRs in clinical conditions under free sound-field stimulation.
Amplitude of steady state response in normal-hearing subjects The amplitude values of ASSR using the multiple frequency technique were collected from all the subjects with normal hearing. The distribution of individual thresholds which contribute to the ASSR amplitude analysis (differentiated between frequencies) is shown in Table 2. The mean and standard deviation of ASSR amplitudes obtained for the stimulation intensities of 60, 50, and 40 dB HL are reported in Table 3. In general, the ASSR amplitudes were between 20 and 90 nV and the highest values correspond to 500 Hz. The values obtained here in normal-hearing subjects are similar to those reported in the literature using headphones transducer with multiple frequency stimuli: between 20 and 100 nV (Lins and Picton, 1995; Pérez-Abalo et al, 2001; Dimitrijevic et al, 2004). A linear correlation between the stimulation intensity and the ASSR amplitude was calculated for each frequency across our sample. For this analysis, the four frequencies explored were treated as independent variables. The results are shown in Figure 1. There was a strong and significant linear correlation frequency by frequency. Note, though, that the lowest regression coefficient (0.3); p ⬍ 0.035 corresponded to 4000 Hz. Similar effects of intensity and ASSR amplitude using headphones transducer and multiple frequency technique were reported by John et al, 2001. Our results show that as the intensity of the stimulus increase, the amplitude of the response increases. This behavior has been described for ASSRs at rates near to 80–100 Hz (Lins et al, 1995), who reported changes in response of approximately 2 nV/dB for intensities below 70 dB SPL. Previous works have reported difficulty in detecting and extracting the ASSR to multiple amplitude modulated tones at low frequencies, especially at 500 Hz (Lins et al, 1995, 1996; Lins & Picton, 1995; Pérez-Abalo et al, 2001; Picton et al, 2004). Based on this literature, we increased the acoustical energy of 500 Hz Table 3. ASSR amplitude under sound field. Thresholds (dB HL)
500 Hz
1000 Hz
2000 Hz
4000 Hz
60 50 40 30
90 ⫾ 40 50 ⫾ 30 30 ⫾ 10
60 ⫾ 20 40 ⫾ 10 20 ⫾ 10 10 ⫾ 4
50 ⫾ 20 30 ⫾ 20 20 ⫾ 10 18 ⫾ 1
40 ⫾ 10 30 ⫾ 10 20 ⫾ 10 15 ⫾ 8
Mean ⫾ SD. All values are expressed in nanovolt (nV).
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Figure 1. The linear correlation between the stimulation intensity and ASSR amplitude in the 20 normal-hearing subjects is shown. A scatter plot diagram is shown for each of the carrier frequencies. The solid line in each plot represents the regression line calculated for each carrier frequency. The frequencies of 500, 1000, and 2000 Hz showed p ⬍ 0.00, and 4000 Hz, p ⬍ 0.035. The ASSR amplitude obtained at 30 dB HL was excluded from this analysis because of the small sample size (see Table 2). (2–4 dB SPL) to generate the multiple frequency stimuli. To check if our compensation had an effect on the ASSR amplitude we compared the values obtained between each frequency. We found significant ASSR amplitude differences between frequencies: F (3, 95) ⫽ 3.54, p ⬍ 0.02. We used a Fisher’s LSD (least significant difference) or planned comparison test to show that the ASSR amplitude to 500 Hz was different from the ASSR amplitude to 2000 Hz and 4000 Hz (p ⬍ 0.001). We are able to conclude that the shift in acoustical energy at 500 Hz increases the ASSR amplitude. Further studies will be needed to compare the ASSR to 500 Hz with and without the acoustical compensation under free sound field conditions.
Conclusions Our experiments provide quantitative evidence on the usefulness of ASSR to multiple amplitude-modulated tones under free-field conditions in assessing auditory thresholds in normal-hearing subjects. Our measurements produced highly consistent results and so are also successful field tests for the AUDIX equipment we have developed. With these baseline data, we are confident that this free sound-field approach will allow us to assess objectively in a clinical setting the amplification gain provided by a cochlear implant or hearing aids
in subjects who cannot reliably respond on behavioral testing. Our recording procedure now needs to be established in subjects with hearing aids and cochlear implants.
Acknowledgements We would like to thank T. Devoogd, A. Lage, E. Martínez, and Y. Iturria for their valuable comments and suggestions while preparing the manuscript. In addition we want to thank to Dr. Durrant for his exceptional help on earlier drafts of the manuscript. Declaration of interest: The authors report no conflict of interest. The authors alone are responsible for the content and writing of the paper.
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