Maximum Length Sequence Auditory Evoked Brainstem Responses in Human Newborns and Adults

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1 J Am Acad Audiol 3 : (1992) Maximum Length Sequence Auditory Evoked Brainstem Responses in Human Newborns and Adults Robert E. Lasky* Jeffrey Perlman' Kurt Hecoxt Abstract Experiment 1 investigated developmental differences at high stimulus rates by using maximum length sequences (MLSs) and cross-correlation techniques to recover auditory evoked brainstem responses (ABRs). Reliable MILS ABRs were recorded in all of the newborns tested at the highest rate presented (minimum interpulse interval = 1.1 msec). Interpreting developmental rate effects from latency and amplitude shifts is problematic. Identification of higher order kernels offers new information concerning developmental rate effects. Kernel slices were measured at lower rates in more adults than newborns, suggesting that the newborn auditory system is less sensitive to temporal nonlinearities than the mature auditory system. This runs counter to developmental rate studies using conventional stimuli. Experiment 2 investigated developmental differences at high rates due to varying stimulus intensities. MLS wave V intensity functions were less steep than conventional wave V intensity functions. MLS thresholds were also higher than conventional thresholds (primarily due to the newborn data). Without equating for signal-to-noise ratio, it is difficult to make unambiguous conclusions concerning the observed developmental differences. Key Words: Auditory brainstem evoked responses (ABRs), auditory evoked potentials, developmental rate effects, maximum length sequences (MLSs), newborns, nonlinear system analysis aximum length sequences (MLSs) and cross-correlation techniques have been M used to record evoked potentials in human adults (Eysholdt and Schreiner, 1982 ; Burkard et al, 1990). These techniques offer at least three advantages relative to conventional signal averaging. If the evoked response exceeds the inter-stimulus-interval (ISI), the signal averaged response is difficult to interpret since evoked responses to successive stimuli overlap. MLSs and cross-correlation techniques *Neurology Department, University of Wisconsin Medical School, Madison, Wisconsin ; +Departments of Pediatrics and Obstetrics and Gynecology, University of Texas Southwestern Medical Center at Dallas, Dallas, Texas and ; t Nicolet Instrument Corporation and Neurology Department, University of Wisconsin Medical School, Madison, Wisconsin Reprint requests : Robert E. Lasky, Neurology Department, University of Wisconsin Medical School, H6-573 Clinical Science Building, 600 Highland Avenue, Madison, W avoid this problem, permitting the presentation of stimuli at higher rates than possible conventionally (Eysholdt and Schreiner, 1982). Second, MLSs can be used to study temporal nonlinearities within the framework of nonlinear systems analysis (Shi and Hecox, 1991). Third, MLSs may be used to investigate the contributing transient responses of steady state potentials (Picton et al, 1991). This study was conducted for two reasons. The first was to determine whether it was possible to record MLS ABRs reliably from normal, term newborns. The second was to use MLS recording techniques to provide novel information concerning developmental differences in auditory processing. Developmental studies addressing temporal nonlinearities (e.g., stimulus rate, temporal masking) have been well documented over the past 15 years (Despland and Galambos, 1980 ; Lasky and Rupert, 1982 ; Lasky, 1984, 1991 ; Cox, 1985). In this study MLS ABRs were re- 383

2 iiml ` I I t1 rllpjw',f 8 Journal of the American Academy of Audiology/Volume 3, Number 6, November 1992 corded in normal term newborns and normal hearing adults to determine developmental differences in temporal nonlinearities at rates exceeding those previously investigated. MLS ABRs permit the specification of the temporal nonlinearities of the developing human auditory system within a nonlinear systems analysis framework (Shi and Hecox,1901). Within this framework nonlinear systems are described by a functional series (Marmarelis and Marmarelis, 1978). The terms of this functional series are called kernels. When the system modeled is linear, the only terms in the series are the zero and first order kernels. Given the input we used in this study (a series of clicks), the first order kernel characterizes the response of the system as the algebraic sum (superposition) of the responses to each click in the input. For nonlinear systems, higher order kernels must be included in the functional series in addition to the zero and first order kernels in order to characterize the response of the system. The ncn order kernel represents the effect on the system response of the interaction among n clicks of the input (i.e., the ncn order kernel indicates the extent that the system response deviates from the superposition of the responses to the n clicks of the input if the system was linear). Comparing newborn and adult auditory systems by the functional series that characterize those systems is a potentially illuminating approach to describing developmental differences. Such a comparison could provide new insights into developmental differences in temporal nonlinearities. For example, interpreting developmental rate effects from latency and amplitude shifts is problematic. A 1 msec wave V latency prolongation as a function of a change in rate does not necessarily mean the same thing for newborns and adults. In contrast, a nonlinear systems analysis description of newborn and adult auditory systems may provide a more informative description of developmental differences in rate effects. Subjects METHOD Healthy normal term newborns and normal hearing young adults served as subjects. The newborns were (1) judged healthy by routine physical and neurologic examinations by the Pediatric House Staff, (2) had 1 and 5 min Apgar scores? 8, (3) were between 37 and 41 weeks post conception according to the Pediatric House Staff's estimate of gestational age based on the Lubchenco (1970) examination, (4) weighed more at birth than the 25"' percentile on the Colorado growth grid, (5) passed an auditory evoked brainstem response screening assessment (90 and 60 db SPL), and (6) without family history of congenital hearing loss. All newborns were vaginal deliveries tested between 24 and 60 hr after birth. The adults were audiologically normal by pure tone audiometry. They had no greater than a 10 db loss at the audiometric frequencies from 0.25 to 8 khz. The adults ranged in age from 17 to 24 years of age (mean = 21 years, SD = 2.1 years). The study was reviewed and approved by The University of Texas Southwestern Medical Center at Dallas Internal Review Board. Permission for newborn study participation was obtained from the parents. Apparatus and Stimuli A microcomputer with a 386 Intel microprocessor interacted with an Ariel 16+ DSP signal processing board to generate the MLSs. The MLSs were a special class of MLSs labelled binary m-pulse sequences (Shi, 1990). MLSs of order six were presented to all subjects. Thus, each sequence consisted of 63 (26-1) binary events (either a pulse or no pulse) separated by a constant interval of silence, the minimum interpulse interval (IPI) characterizing the sequence. Thirty-two events of the sequence were pulses, and 31 were no pulses. The pulses were 100 sec clicks. Half of the pulses were separated by the minimum IPI and the remaining pulses were separated by integer multiples of the minimum IPI. The amplitude of the pulses (the intensity of the sequence) and the minimum IPI (the duration of the sequence) could vary. The intensity of the pulses constituting the MLS was defined by measuring the intensity of the pulses in peak db SPL(A) presented at 10/sec using a Bruel and Kjaer Artificial Ear (Type 4152) and a Bruel and Kjaer measuring amplifier (Type 2610). In Experiment 1 the minimum IPI was varied. In Experiment 2 the intensity of the stimuli was varied. The MLS was presented repeatedly and the responses to the MLSs were averaged to improve the SNR before the cross-correlation operation was performed. The MLSs were presented continuously with no interval between sequences until responses to 200 sequences 384

3 MLS ABRs in Newborns and Adults/Lasky et al were averaged. If the input exceeded ± 20 pv during a presentation of the MLS, the response to that sequence was rejected and not included in the average. Three gold plated cup electrodes were attached at the vertex (+), the mastoid (-), and the forehead (ground) with impedances between any two electrodes less than 10,000 S2. The responses were amplified 200,000 times and filtered with the 1/-2 amplitude cut-offs at 100 Hz and 3 khz respectively (Grass P511 K preamplifier). The roll-offs were 18 db/octave. The Ariel 16+ DSP signal processing board was used to digitize the analog response with a sampling rate of 10 khz. The averaging of the response and the cross-correlating of the recovery sequence was calculated by the host computer. The same equipment was used to present a constant IPI series of pulses (the same 100 psec clicks used in the MLS) and record ABRs by signal averaging the responses to 2000 clicks. We labelled these conventional ABRs. Stimulus rate was varied in Experiment 1, and the intensity (calibrated in the same way as for the MLSs) was varied in Experiment 2. The sampling rate was 10 khz, the same as for the MLS ABRs. Replicate responses were recorded to each stimulus presented to each subject. The latency and amplitude of wave V (first order kernels) were scored independently for each waveform. Wave V was selected as the response of interest since it is the most reliable of the ABR waves and the most robust in terms of intensity and rate effects (Lasky et al, 1987). In addition, the latency and amplitude of the most prominent wave of the first and second slices of the second order kernel and the first slice of the third order kernel were measured from each cross-correlation function. One of the advantages ofusingthe pseudorandom sequence we used is that all of the higher order kernel slices recoverable can be recovered from a single cross-correlation operation (Sutter and Vaegen, 1990). We focused on the kernel slices mentioned above since they had been most prominent in preliminary studies. The presence and absence of kernel slices are a consequence of the temporal nonlinearities that characterize the auditory system. If the auditory system were linear, only the zero and first order kernel would be present. If it were a second order system, the second order kernels would also be present. If it were a third order system, the third order kernels would also be present, and so on. A second order system is affected by the temporal interactions between two pulses. The first slice of a second order kernel refers to the effect on the response to a pulse of another pulse that precedes the first by the minimum IPI. The second slice of a second order kernel refers to the effects on the response to a pulse of another pulse that precedes the first by twice the minimum IPI. Similarly, a third order system is affected by the temporal interactions among three pulses. The first slice of a third order kernel refers to the effects on the response to a pulse preceded by two pulses with the minimum IPI separating each of the three pulses in sequence. Testing was conducted in a quiet room. For the newborns the quiet room was in the Parkland Memorial Hospital Newborn Nursery ; for the adults it was in a quiet room in a laboratory at Nicolet Instrument Corporation. E EXPERIMENT 1 xperiment 1 investigated developmental differences at high stimulus rates by using MLSs. Consequently, the rates presented exceed those possible using signal-averaged evoked potentials. As such they provide novel information concerning temporal nonlinearities in human newborns and adults. Ten newborns and 14 adults participated in Experiment 1. Four MLS rates were presented to each subject (minimum IPIs = 10.2, 4.4, 2.2, and 1.1 msec). Three conventional rates were presented to each subject (IPI = 50.1, 20.4, and 10.2 msec). All the stimuli were presented at 90 db SPL. RESULTS igure 1 presents examples of conventional and MLS ABRs from a newborn and an F adult subject. Replicate responses are represented. Figures 2 and 3 present wave V latency x rate and wave V amplitude x rate functions respectively. A 2 (age) x 7 (rate) repeated measures analysis of variance was computed separately for the MLS wave V latency and amplitude measurements. The age [F (1,22)= ; p <.001 and F (1,22) = ; p <.0011 and the rate [F (6,132) = ; p <.001 and F (6,132) = ; p <.0011 main effects were significant for wave V latencies and amplitudes respectively. Adult wave Vs were shorter in latency and larger in amplitude than newborn wave Vs 385

4 Journal of the American Academy of Audiology/Volume 3, Number 6, November 1992 Newborn Adult Figure 1 An example of conventional and MLS ABRs from a newborn and an adult subject. Conventional IS1= 10.2 ms MLS minimum IPI= 10.2 ms 4.4 ms..aa,, 2.2 ms 1.1 ms at all rates. For both newborns and adults wave V latency increased and wave V amplitude decreased with increasing stimulus rate. Although the wave V latency age x rate interaction was not significant at the.05 level, the wave V amplitude age x rate interaction was significant [F (6,132) = ; p < Increasing rate had a greater effect (reduced amplitude) on adult wave V amplitudes than newborn wave V amplitudes. As a function of rate, Table 1 presents the number of subjects who had replicable first and second slices of the second order kernel and first slices of the third order kernel. These kernels had been identified as the most prominent kernel slices in preliminary studies. The presence of all three kernel slices increased as stimulus rate increased. As expected, a greater percentage of subjects and at slower rates had a first slice of the second order kernel, followed by second slices of the second order kernel, with the smallest percentage of subjects, and at only the fastest rates having a first slice of the third kernel. At each rate for each kernel slice chi squares were calculated to investigate developmental differences. The Yates correction was used. Significant development differences are noted in Table 1. Generally, a greater percentage of adults at slower rates had kernel slices compared to newborns. Because of missing data due to the absence of kernel slices, analyses concerning kernel slice latencies and amplitudes were not conducted. E EXPERIMENT 2 xperiment 2 investigated developmental differences due to intensity effects at high rates using MLSs. Again, the information recorded is novel since the rates presented exceed those previously presented to newborns and adults. Ten newborns and 10 adults participated as subjects in Experiment 2. Each subject was presented two intensity series, one conventional and one MLS. The conventional stimuli were presented at an IPI = 20.4 msec. The MLS stimuli were presented at a minimum IPI = 2.2 msec. Two replicate waveforms were collected to each stimulus. In each case, the stimuli were first presented at 90 db SPL. For the adults, 386 A II IrI11i.

5 MLS ABRs in Newborns and Adults/Lasky et al ---at- newborn conv t newborn MLS -tr- adult conv -4- adult MLS -~ newborn conv --d'- adult conv t newborn MLS --4- adult MLS Figure 2 Wave V latency x rate functions for human newborns and adults. Figure 3 Wave V amplitude x rate functions for human newborns and adults. the intensity of the stimulus was decremented in 10-dB steps until no reproducible responses were recorded. In an effort to reduce the length of the recording session for the newborns, the intensity of the stimulus was decremented in 20-dB steps. After recording the first subthreshold response, the intensity of the stimulus was increased 10 db ; and two more replicate waveforms were collected. RESULTS inear functions were calculated for each L subject with all available data for wave V latency x intensity and amplitude x intensity functions. Table 2 presents the mean (SD) slopes of the latency x intensity and amplitude X intensity functions by age of the subject and type of ABR. The percentage of the variance explained indicates that linear functions adequately described these functions. Two (age) x 2 (type of ABR) repeated measures analyses of variance were calculated to determine developmental differences in these functions. There was a significant type of ABR main effect for wave V latency [F (1,18) = ; p < There were significant age [F (1,18) = ; p =.0031 and type of ABR [F (1,18) = ; p <.0011 main effects for wave V amplitudes. Conventional wave V latency and amplitude x intensity functions were steeper than MLS wave V latency and amplitude functions. Adults had signifi- Table 1 The Number of Subjects with Kernel Slices as a Function of Age and Rate Minimum Newborns Adults IPI(msec) Absent Present Absent Present First Slice Second Kernel Second Slice Second Kernel First Slice Third Kernel p <

6 Journal of the American Academy of Audiology/Volume 3, Number 6, November 1992 Table 2 Mean (SD) s of the Wave V Latency x Intensity and Amplitude x Intensity Functions by Age and Type of ABR Conventional R2 Newborn MLS R' Conventional R2 Adult MLS R` Wave V Amplitude z SD n Wave V Latency x SD n cantly steeper wave V amplitude x intensity functions than newborns. ABR threshold responses were specified for each subject for both conventional and MLS ABRs. Figure 4 presents these data. A 2 (age) x 2 (type of ABR) repeated measures analysis of variance was calculated to contrast ABR thresholds as a function of age and type of ABR. There were significant age [F (1,18) = ; p =.005] and type of ABR [F (1,18) = 4.74 ; p =.0431 main effects. Newborns had higher thresholds than adults. MLS thresholds were higher than conventional thresholds. This latter result was clearly due to the newborns although the age x type of ABR interaction was nonsignificant. T DISCUSSION his study recorded MLS ABRs in human newborns and adults. Interest in recording MLS ABRs in human newborns is motivated by both clinical and research concerns. MLS evoked potentials can be used to study rate effects that are a reflection of an important physiological process. Reliable MLS ABRs were recorded in all of the newborns tested at the highest rate presented (minimum IPI = 1.1 msec). It is possible to present even higher rates using MLSs. There may be human developmental differences in the refractory period of the neurons of the auditory tract. MLS evoked potentials may be one way to study them. As expected from conventional rate studies, newborn MLS wave V ABRs were longer latency and smaller amplitude than adult MLS wave V ABRs at all rates assessed. Unexpectantly, however, the wave V latency age x rate interaction was not significant. That is, newborn wave Vs were not significantly more prolonged as rate increased than adult wave V latencies. A wave V latency age x rate interac- tion is commonly reported in the literature (Despland and Galambos, 1980 ; Lasky, 1984 ; Cox, 1985). In contrast, there was a significant age x rate interaction for wave V amplitude. As for conventional rates (Lasky,1984), adult wave V amplitudes reduced significantly more rapidly than newborn wave V amplitudes as a function of increasing rate. The kernel slice data offer new information concerning developmental rate effects. Kernel slices were measured at slower rates in more 6 5 Adult Thresholds Number 4 aa,.ns-mis of subjects db SPL Newborn Thresholds Number 4 ~ ~awbo,~=-~on~ of subjects db SPL newbams-mls Figure 4 Newborn and adult conventional and MLS ABR thresholds. 388 ill,.l ~, ~ }Kpllii~ =llulr~ll~rj~

7 MILS ABRs in Newborns and Adults/Lasky et al adults than newborns. If anything, these data suggest that the newborn auditory system is less sensitive to rate effects at high rates than the mature auditory system. This runs counter to conventional developmental rate studies (Despland and Galambos, 1980 ; Lasky, 1984 ; Cox, 1985). One qualification concerns distinguishing the failure to detect a kernel slice from failure to evoke that kernel slice. Without equating for signal-to-noise ratio (SNR), it is difficult to make unambiguous conclusions. That is the case with the present study. Similar comments can be made about the intensity series data. Specifically, MLS wave V intensity functions were steeper than conventional wave V intensity functions. MLS thresholds were also higher than conventional thresholds (this result seems to be due to the newborn data although it is not possible to make a definitive statement because of insufficient statistical power). Again, without equating for signal-to-noise ratio (SNR), it is difficult to make unambiguous conclusions concerning intensity functions. This study demonstrates that MLS ABRs can be recorded from human newborns over a wide range of rates and intensities. The rates presented exceed those used conventionally, and, consequently, provide novel information concerning temporal nonlinearities. Specifying the newborn system by order (kernel) and memory length (slice) permits a parsimony and rigor of description not yet achieved in human developmental research concerning the auditory system. A number of issues remain to be addressed in order to interpret MLS ABRs in newborns meaningfully. One of these concerns has to do with SNR. SNR obviously affects the ability to identify the presence and reliability of a response. Until SNR issues are more systematically addressed, conclusions concerning differences in ABR thresholds as a function of variables such as age and type of signal processing (e.g., conventional or MLS) must be qualified. REFERENCES Burkard R, Shi Y, Hecox KE. (1990). Brainstem auditory evoked responses elicited by maximum length sequences : effects of simultaneous masking noise. JAcoust Soc Am 87: Cox LC. (1985). Infant assessment : developmental and age-related considerations. In : Jacobson JT, ed. The Auditory Brainstem Response. San Diego : College-Hill Press, Despland PA, Galambos R. (1980). The auditory brainstem response is a useful diagnostic tool in the intensive care nursery. Pediatr Res 14 : Eysholdt U, Schreiner C. (1982). Maximum length sequences-a fast method for measuring brain-stem-evoked responses. Audiology 21 : Lasky RE. (1984). A developmental study on the effect of stimulus rate on the auditory evoked brainstem response. Electroencephalogr Clin Neurophysiol 59 : Lasky RE. (1991). The effects of rate and forward masking on human adult and newborn auditory evoked brainstem response thresholds. Dev Psychobiol 24 : Lasky RE, Rupert A. (1982). Temporal masking of auditory evoked brainstem responses in human newborns and adults. Hear Res 6: Lasky RE, RupertA, Waller M. (1987). Reproducibility of auditory brainstem evoked responses as a function of the stimulus, scorer, and subject. Electroencephalogr Clin Neurophysiol 68 : Lubchenco L. (1970). Assessment of gestational age and development at birth. Pediatr Clin North Am 17 : Marmarelis PZ, Marmarelis VZ. (1978). Analysis of Physiologic Systems. New York : Plenum Press. Picton T, Champagne S, Kellet A. (1991). Personal communication. Shi Y. (1990). M-pulse Sequences in the Study of Nonlinear Behavior ofauditory Evoked Potentials. Doctoral Thesis, University of Wisconsin, Madison. Shi Y, Hecox K. (1991). Nonlinear system identification by m-pulse sequences : application to brainstem auditory evoked responses. IEEE Trans Biomed Eng 38 : Sutter E, Vaegen. (1990). Lateral interaction component and local luminance nonlinearities in the human pattern ERG. Vision Res 30 : Acknowledgment. Portions of this manuscript were presented at Recent Advances in Audiology, July 26, 1991, Hanover, New Hampshire and The American Speech, Language and Hearing Association Convention, November 23, 1991, Atlanta, Georgia. This work was supported by grant #R01 NS and Nicolet Instrument Corporation.

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