Effects of Stimulus Phase on the Latency of the Auditory Brainstem Response

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1 J Am Acad Audiol 2 : 1-6 (1991) Effects of Stimulus Phase on the Latency of the Auditory Brainstem Response Michael P. Gorga Jan R. Kaminski Kathryn L. Beauchaine Abstract Auditory brainstem responses were measured in five normal-hearing subjects, using singlecycle sinusoids at octave frequencies ranging from 250 to 2000 Hz. These sinusoids, gated with Blackman functions, were presented either at 0 or 180 degree phase and were varied in level from 90 db SPL to threshold in 10-dB steps. Stimulus phase affected wave V latencies for low-frequency stimuli, with the effect decreasing as frequency increased. These data are thought to represent an evoked potential manifestation of known phase-locking abilities within the auditory system. Key Words: Auditory brainstem response (ABR), single-cycle sinusoids, phase, wave V latency, frequency-dependent phase effects T here has been considerable debate regarding the effects of stimulus phase or polarity on the auditory brainstem response (ABR). There does not appear to be a consensus on whether any effects exist, and, if they exist, on the magnitude or the direction of polarity effects on ABR latencies. In normal-hearing subjects, there are studies that report no effect of click polarity, other studies report shorter latencies for rarefaction clicks, while still others report shorter latencies for condensation clicks (e.g., Terkildsen et al, 1973 ; Coats and Martin, 1977 ; Stockard et al, 1978 ; Beattie and Boyd, 1984). Even those studies reporting significant polarity effects find a very small effect, typically less than 0.1 msec. Data from hearing-impaired subjects, however, suggest that larger polarity effects may occur under some conditions in cases of high-frequency hearing loss. For example, Coats and Martin (1977) reported significantly longer latencies of the wholenerve action potential for condensation clicks compared to rarefaction clicks. However, this effect was much less obvious in measurements of wave V latencies. Pijl (1987) also reported longer latencies Boys Town National Research Hospital, Omaha,- Nebraska Reprint requests : Michael P. Gorga, Boys Town National Research Hospital, 555 North 30th Street, Omaha, NE for condensation clicks. In both studies, the effect appeared to be related to the magnitude of highfrequency hearing loss, such that greater effects were observed as hearing loss increased. The fact that little or no effect of click polarity on ABR latencies is observed in normal subjects and that larger effects are observed in patients with high-frequency hearing loss suggests a simple hypothesis. Specifically, cochlear hearing loss may alter the effective spectrum of the stimulus, such that the relative contributions to a gross response from different cochlear regions are not the same in normal subjects and patients with high-frequency hearing loss. This hypothesis is based upon three assumptions. Firstly, high-frequency cochlear regions dominate the response in normal-hearing subjects ; secondly, high-frequency hearing loss results in less high-frequency contributions to the response so that low-frequency regions contribute relatively more to the response ; and thirdly, phase or polarity effects are predominantly low-frequency effects. It is widely recognized that high-frequency cochlear regions dominate gross potential recordings. For example, Jerger and Mauldin (1978), Gorga et al (1985b), and van der Drift et al (1987) reported the highest correlation between clickevoked ABR thresholds and the behavioral thresholds for 2000 and 4000 Hz. Thus, the first assumption would appear valid.

2 Journal of the American Academy of Audiology/Volume 2, Number 1, January 1991 Evidence also exists supporting the idea that a relatively larger contribution from low-frequency cochlear regions is observed in cases of highfrequency hearing loss. The observation of longer absolute latencies in cases of high-frequency hearing loss provides indirect support for this argument. Furthermore, it is widely recognized that response latency is related to cochlear place, such that longer latencies are observed for apical (lowfrequency) regions compared to basal (high-frequency) regions (e.g., Kiang et al, 1965 ; Kiang, 1975). Both Coats and Martin (1977) and Gorga et al (1985b) noted steeper wave V latency-intensity functions in patients with high-frequency hearing loss. That is, more normal response latencies were observed at high stimulus intensities, but abnormally prolonged latencies were observed for lower intensities. This pattern of response suggests that, for some hearing-impaired patients, the cochlear regions generating the dominant contribution to the response might be changing with intensity (Gorga et al, 1985a, b). Thus, the second assumption would appear reasonable as well. Finally, physiologic studies exist that demonstrate phase (polarity) sensitivity in the auditory nerve. In addition to increasing their rate in the presence of an excitatory stimulus, auditory neurons also demonstrate an ability to "phase-lock" to the stimulus, such that one phase (or polarity) causes an increase in discharge rate (depolarization) while the opposite phase causes a reduction in rate (hyperpolarization) (Rose et al, 1967 ; Johnson, 1980 ; McGee, 1983 ; see Javel, 1986 and Javel et al, 1988 for reviews). This phase-locking ability is a predominantly low-frequency effect and is reduced or absent for frequencies exceeding 2000 Hz. Thus, the final assumption necessary to account for the differences in polarity effects for normal and hearing-impaired subjects also would appear reasonable. If these assumptions are correct, then one would predict that polarity (or phase) would alter response latencies in those cases when the response is dominated by the low-frequency components in the stimulus, regardless of whether hearing is normal or not. In this regard, however, conflicting data have been reported. Salt and Thornton (1984) varied the rise time of clicks, thus altering their amplitude spectra. Clicks with longer rise times have greater low-frequency energy. They observed little or no effect of polarity on ABR latencies for any rise times. Thus, using a low-frequency stimulus did not result in predicted effects of polarity on latency. Moller (1986) measured whole-nerve action potentials in rats, using either broadband clicks, low-pass filtered clicks, or a combination of these stimuli. He observed significant polarity effects for stimuli containing greater low-frequency energy. Thus, his findings are more consistent with the expectations based on the known phase-locking properties of the auditory system, but differ from those reported by Salt and Thornton (1984). The reasons for these differences are not obvious. It was the purpose of the present study to provide more data related to the effects of stimulus polarity on ABR latencies in an effort to determine whether evidence of polarity sensitivity, known to exist at the level of individual auditory neurons, can be found in gross potential recordings. In this study, we measured normal response latencies for single-cycle sinewaves ranging in frequency from 250 to 2000 Hz. If polarity affects latency in these gross potentials as it does in auditory neurons and if an interaction exists between frequency and polarity effects, one would predict large polarity effects for low-frequency stimuli, with decreasing effects as frequency increased. Subjects METHOD Five normal-hearing young adults served as subjects. Each subject had pure-tone audiometric thresholds less than or equal to 10 db HL (re : ANSI, 1969) for octave frequencies from 250 to 8000 Hz, and had normal tympanometric functions. In addition, all subjects had no history of neurologic dysfunction. Stimuli Stimuli consisted of digitally-generated (40 k sampling rate), single-cycle sinusoids at octave frequencies from 250 to 2000 Hz. Thus, total stimulus duration ranged from 4 msec (250 Hz) to 0.5 msec (2000 Hz). Stimulus amplitude was varied from 90 db peak equivalent SPL (re : 28 ppa peak pressure) down to threshold in 10-dB steps. These single-cycle sinewaves were presented at either 0 or 180 degrees. That is, the initial portion of the sinewave was characterized either by a positive-going zero crossing (0 degree) or a negativegoing zero crossing (180 degrees). All sinusoids were gated with Blackman functions (Harris, 1978 ; Nuttall, 1981), and were presented at a rate of 39/sec. Time waveforms (inserts) and amplitude

3 Effects of Stimulus Phase on Latency of ABR/Gorga et al spectra for these stimuli are shown in Figure 1. Note that although the 250-Hz toneburst has a broad spectrum, energy is restricted to frequencies below about 600 Hz. Stimuli were delivered via an insert earphone (Etymotic, ER-3A). Procedures ABRs were measured between chlorided silver-silver disc electrodes affixed to the vertex and ipsilateral mastoid. Both electrodes were referred to a ground electrode placed at the forehead. EEG activity was amplified (100,000), filtered (100 to 3000 Hz, 6 db/octave), and digitized (25 psec dwell time) prior to input to an averager (Nicolet, 1170). Responses to 2048 stimulus presentations were included in each averaged response, which was replicated once. Z O O m RESULTS igure 2 shows response waveforms from one F subject for the 250-Hz stimulus. A different intensity is represented in each panel. Within each panel, the top two superimposed traces represent the responses obtained at 180 degrees, the middle two superimposed traces represent responses for 0 degree phase stimuli, and the bottom pair of traces represent the sum of the responses for 0 and 180 degree phase stimuli. This latter condition is equivalent to the response that would have been obtained if stimuli were presented with alternating polarity (phase) in a single run. Clearly, response latency depends on stimulus polarity for this 250-Hz toneburst. Well-formed responses were observed for both stimulus phases, although the responses were not identical. Notably, wave V latencies were systematically longer for stimuli presented at 0 degrees. Finally, adding the responses for stimuli of opposite phase sometimes had a negative effect on response clarity, especially for low-intensity stimuli, often obscuring the point at which response latency was taken. Figure 3 represents data from another subject for a 2000-Hz stimulus. Again, clear response waveforms were observed for both stimulus phases. In this case, however, there is no obvious effect of phase on latency. Indeed, response waveforms appear virtually identical, regardless of stimulus phase, at each of these four intensities. As a consequence, adding the responses for op db SPL 70 db SPL Y 0 SUM W Y 80 db SO PL Y 60 db SPL I gyp- ~- ~c~ Y FREQUENCY IN khz Figure 1 Time waveforms (inserts) and amplitude spectra for tone burst stimuli. All stimuli were singlecycle sinusoids gated with Blackman windows. Figure 2 Auditory brainstem responses from one subject in response to 250-Hz tone bursts. Results from a different intensity are shown in each panel. Within each panel, the top pair of traces represent responses to 180 degree phase stimuli, the middle pair represent responses to 0 degree phase stimuli, and the bottom pair represent the sum of the responses to these opposite phase stimuli.

4 Journal of the American Academy of Audiology/Volume 2, Number 1, January 1991 Figure 3 Auditory brainstem responses from one subject in response to 2000-Hz tone bursts. Results from a different intensity are shown in each panel. Within each panel, the top pair of traces represent responses to 180 degree phase stimuli, the middle pair represent responses to 0 degree phase stimuli, and the bottom pair represent the sum of the responses to these opposite phase stimuli. 250 Hx 500 H: L 6-- ~ 1000 Hz 2000 H: B Intensity (db SPL) Figure 4 Mean wave V latency (msec) (±1 standard deviation) as a function of intensity (db SPL). Each panel represents data for a different frequency. Within each panel, results with 180 degree phase stimuli are shown as open symbols, while data obtained in response to 0 degree phase stimuli are shown as filled symbols. Intensity (db SPL) Figure 5 Mean latency differences (msec) as a function of intensity when wave V latencies for 180 degree phase stimuli are subtracted from the latencies for 0 degree = phase stimuli. The parameter is stimulus frequency : V 250 Hz ; 0 = 500 Hz ; /A= 1000 Hz ; D =2000 Hz. as frequency increases. The effects of phase are not apparent for the 2000-Hz stimuli. Finally, Figure 5 shows the mean differences in latency between stimuli of opposite phase as a function of intensity, with stimulus frequency as the parameter. As noted above, the effects of phase are greatest for 250 Hz, decreasing for higher frequencies. The predicted difference at 250 Hz cannot exceed 2 msec, which is the difference in time between each half cycle of the sinewave. In this case the difference in latency ranged from about 1 msec up to about 1.5 msec. At 500 Hz, the difference ranged from about 0.2 msec to 0.75 msec. For both 1000 Hz and 2000 Hz, the differences vacillate around 0 msec. Thus, these data confirm an effect of polarity on latency that decreases as frequency increases. The reason for the intensity dependence of this effect is not known. DISCUSSION posite phase stimuli did not result in a more ambiguous waveform. In fact, the response should be improved slightly because of the 3-dB improvement in signal (response)-to-noise ratio that is achieved with a doubling of the number of stimuli. Figure 4 displays average wave V latencies (±1 standard deviation) as a function of intensity for all five subjects. Each panel represents data for a different frequency, and within each panel, the parameter is stimulus phase. Note that large effects of phase are obvious at 250 Hz, decreasing T he results of this study suggest that phase and, by extension, polarity will affect latencies for those stimulus conditions in which the response is dominated by low-frequency energy. For conditions in which the response is dominated by high-frequency energy (as in the case when 100- psec clicks are used to elicit responses from normal-hearing subjects), no effects of polarity should be expected. These findings are completely consistent with the known behavior of individual hair cells and neurons within the auditory pathway.

5 Effects of Stimulus Phase on Latency of ABR/Gorga et al For example, it is well known that hair cells are excited when their stereocilia are bent in one direction and are inhibited when they are bent in the opposite direction (Hudspeth and Corey, 1977). Manifestations of this phase sensitivity have been reported in the responses of neurons throughout the auditory pathway (e.g., Goldberg and Brown, 1969 ; Rose et al, 1967 and 1974 ; Johnson, 1980 ; McGee, 1983). The fact that these phase effects occur predominantly for low frequencies also has been demonstrated (Johnson, 1980 ; McGee, 1983 ; Javel, 1986). Our findings thus agree with the evokedpotential observations made by Moller (1986), but are at odds with those reported by Salt and Thornton (1984). While both our data and those reported by Moller can be accounted for in the context of underlying physiologic response properties, the results reported by Salt and Thornton are more difficult to explain. Clearly, there are other differences between these three studies. For example, the previous studies used either clicks with different rise times or filtered clicks to obtain a stimulus set whose spectra varied. We opted to use single-cycle sinewaves because predictions regarding the magnitude of the phase effect are simple with such stimuli. Still, it is not clear why these differences in stimuli would account for different polarity effects observed in these studies. It may be of some interest to speculate on why similar effects are sometimes observed for click stimulation in hearing-impaired subjects. If the hearing loss shapes the effective stimulus such that low-frequency components (and therefore, more apical regions of the cochlea) provide relatively larger contributions to the response, then polarity effects might be observed for the exact same reasons that low-frequency phase effects are observed in normal-hearing subjects. The low-frequency components in a broadband stimulus, such as a 100-psec click, might contribute more to the response in cases of high-frequency hearing loss. Response latencies would be more dependent on stimulus polarity under these conditions. This hypothesis is entirely consistent with a model we use to account for the fact that steep wave V latency-intensity functions are sometimes observed in patients with high-frequency hearing loss (Gorga et al, 1985a, b). This model is based on the fact that response latency is related to the cochlear place generating the response (Kung et al, 1965 ; Mang,1975). The observation of normal (or at least more normal) latencies at high intensities (at least in cases of moderate high-frequency hearing loss), with abnormally prolonged responses at lower levels suggests that the cochlear place(s) contributing to the response has moved toward the apex as intensity decreases. Thus, there is a greater contribution from low-frequency cochlear regions in cases of high-frequency hearing loss. Under those circumstances, polarity effects might be anticipated. The data reported in this study suggest that routinely summing the response to stimuli of alternating polarity, especially for low frequencies, may not always be the best approach clinically. Furthermore, in cases of high-frequency hearing loss, the responses from broadband stimuli having opposite polarity might differ in latency. Adding these responses together might obscure component identification. Thus, a more conservative approach might be one in which responses from opposite polarities are kept separate and are added only for those conditions when such an approach might be needed, such as when one is trying to reduce or eliminate stimulus artifact. The present results also suggest another interesting application for the stimuli used in this study. It is generally accepted that it is more difficult to obtain ABRs to low-frequency stimuli. For example, using gated sinusoids of opposite polarity, we were less successful eliciting ABRs for frequencies below about 1000 Hz (Gorga et al, 1988). The responses we obtained in the present study, using a single-cycle 250-Hz tone burst offixed phase, were very well formed and easily identified down to 60 db SPL (re : 28 ppa). This represents a level of 34 db HL (re : ANSI, 1969). In units comparable to those used routinely to quantify stimulus intensity in clinical ABR measurements (i.e., db HLn), this value would be equivalent to no more than 0 to 10 db. Recall that although this stimulus had a broad spectrum, there was little energy above 600 Hz. Thus, this stimulus might be particularly useful to obtain an estimate of low-frequency sensitivity because it is able to elicit fairly robust responses at relatively low intensities. In fact, one approach might be to measure a click-evoked, wave V threshold and latency-intensity function to obtain an estimate of high-frequency sensitivity and configuration of hearing loss (Gorga et al, 1985a, b), and to measure response threshold to a single-cycle 250-Hz tone burst in order to obtain an estimate of hearing sensitivity for low frequencies. Such an approach should provide information from a wide range of frequencies in the least amount of time. However, the data from the present study suggest that one will be more successful at obtaining responses to tow-frequency stimuli of fixed phase or polarity.

6 Journal of the American Academy of Audiology/Volume 2, Number 1, January 1991 Acknowledgments. This work was supported in part by NIH. We thank Ann Karasek and Steve Neely for their comments on an earlier version of this paper as part of our internal review process. Betsy From is thanked for her help in manuscript preparation, and Pam Cates is thanked for help in preparing figures. REFERENCES American National Standards Institute. (1969). Specifications for Audiometers. ANSI S (R1973). New York : American National Standards Institute. Beattie RC, Boyd R. (1984). Effects of click duration on the latency of the early evoked potentials. J Speech Hear Res27: Coats AC, Martin JL. (1977). Human auditory nerve action potentials and brainstem evoked responses. Arch Otolaryngol 103 : Goldberg JM, Brown PB. (1969). Responses of binaural neurons of the superior olivary complex to dichotic tonal stimuli : some physiological mechanisms of sound localization. JNeurophysiol 32 : Gorga MP, Kaminski JR, Beauchaine KA, Jesteadt W. (1988). Auditory brainstem responses to tone bursts in normally hearing subjects. J Speech Hear Res 31 : Gorga MP, Reiland JK, Beauchaine KA. (1985a). Auditory brainstem responses in a case of high-frequency conductive hearing loss. J Speech Hear Disord 50: Gorga MP, Worthington DW, Reiland JK, Beauchaine KA, Goldgar DE. (1985b). Some comparisons between auditory brainstem response thresholds, latencies, and the pure-tone audiogram. Ear Hear 6 : Harris FJ. (1978). On the use of windows for harmonic analysis with the discrete Fourier transform. IEEE Trans Acoustics Speech Signal Processing 66 : Hudspeth AJ, Corey D. (1977). Sensitivity, polarity, and conductance in the response of vertebrate hair cells to controlled mechanical stimuli. Proc Natl Acad Sci 74 : Javel E. (1986). Basic response properties of auditory nerve fibers. In : Altschuler RA, Hoffman DW, Bobbin RP, eds. Neurobiology of Hearing : The Cochlea. New York: Raven Press, Javel E, McGee J, Horst JW, Farley GR. (1988). Temporal mechanism in auditory stimulus coding. In : Edelman GM, Gall WE, eds. Functions of theauditory System. New York: Wiley, Jerger J, Mauldin L. (1978). Prediction of sensorineural level from the brainstem evoked response. Arch Qtolaryngol 104: Johnson DH. (1980). The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. JAcoust SocAm 68 : Kiang NY-S. (1975). Stimulus representation in the discharge patterns of auditory neurons. In : Eagles EL, ed. The Nervous System. Volume 3 : Human Communication and Its Disorders. New York : Raven Press, Kiang NY-S, Watanabe T, Thomas EC, Clark LF. (1965). Discharge patterns of single fibers in the cat's auditory nerve. MIT Research Monograph No. 35, Cambridge : MIT Press. McGee J. (1983). Phase locking as a frequency and intensity coding mechanism in auditory nerve fibers. Master's thesis, Creighton University. Moller AR. (1986). Effect of click spectrum and polarity on round window NlN2 response in the rat. Audiology 25 : Nuttall AH. (1981). Some windows with very good sidelobe behavior. IEEE Trans Acoustics Speech Signal Processing 29 : Pijl S. (1987). Effects of click polarity on ABR peak latency and morphology in a clinical population. JOtolaryngol 16 : Rose JE, Brugge JF, Anderson DJ, Hind JF. (1967). Phase-locked responses to low-frequency tones in single auditory nerve fibers of the squirrel monkey. J Neurophysiol 30 : Rose JE, Gibson MM, Kitzes LM, Hind JF. (1974). Observations on phase-sensitive neurons of anteroventral cochlear nucleus of the cat : nonlinearity of cochlear output. JNeurophysiol 37 : Salt AN, Thornton ARD. (1984). The effect of stimulus rise time and polarity on the auditory brainstem responses. Scand Audiol 13 : Stockard JJ, Stockard JE, Sharbrough FW. (1978). Nonpathologic factors influencing brainstem auditory evoked potentials. Am J EEG Technol 18 : Terkildsen K, Osterhammel P, Huis in't Veld F. (1973). Electrocochleography with a far-field technique. Scand Audiol 2: van der Drift JFC, Brocaar MP, vanzanten GA. (1987). The relation between the pure-tone audiogram and the click auditory brainstem response threshold in cochlear hearing loss. Audiology 26 :1-10.

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