Ipsilateral and Contralateral Click-evoked Acoustic Reflex Thresholds in Humans

Using stimuli similar to those used in TEOAE and ABR recordings

Measurement of the acoustic reflex has several applications in audiology and hearing health care. It can be used to estimate hearing levels and fit hearing aids in difficult-to-test populations, such as infants and cognitively impaired adults. The ipsilateral acoustic reflex can be a useful hearing screening tool if multiplex stimuli (alternate presentations of probe and reflex activating stimuli) are used in recording the reflex.¹ The reflex can be used in monitoring Cisplatin ototoxicity in the pediatric population. It can help in confirming the presence of a non-organic hearing impairment and evaluating facial nerve pathology. The acoustic reflex can also be useful in determining the site of lesion (conductive, sensorineural, auditory nerve, and low brain stem) in the auditory pathway.

Ipsilateral versus Contralateral Acoustic Reflex

The acoustic reflex can be recorded in either the ipsilateral mode (reflex-activating and probe stimuli in the same ear) or the contralateral mode (activator stimuli in the ear contralateral to that of the ear with the probe stimulus). It is recorded by measuring the changes in middle ear admittance caused by the activation of the stapedius muscle in response to intense auditory stimuli. Recording of both the ipsilateral and contralateral reflexes is known to provide diagnostic information in otoneurology.

The morphologies of the crossed and uncrossed acoustic reflex waveforms can differ. The acoustic reflex thresholds can be lower for the ipsilateral than those for the contralateral mode.²-6 However, other investigators have reported symmetrical acoustic reflex findings in the ipsilateral and contralateral modes.^7,8 Thus, the effect of the ipsilateral and contralateral activation on the acoustic reflex is somewhat controversial.

Acoustic Reflex Activation With Clicks

Most previous studies related to acoustic reflex have used tonal or broadband noise activators to elicit the reflex. Click stimuli have rarely been used in such investigations.

Click-activated acoustic reflex measures can enhance the applications of acoustic reflex in a variety of ways. Such measures can allow us to predict the possibility of the occurrence of reflex during otoacoustic emission (OAE) and evoked potential (EP) measurements, since clicks are frequently used during these measures.

Whitehead et al⁹ showed that the activation of the crossed reflex can reduce the amplitudes of the distortion-product OAEs. It has been suggested that the neural system can be stressed beyond its functional capacity by increasing the click repetition rate, and such stress may reveal subtle auditory neuropathologies.¹⁰ Thus, the interaural difference criteria in acoustic reflex thresholds¹¹ can be improved by comparing acoustic reflex thresholds obtained at various repetition rates on the normal side with those obtained on the side of the suspected nerve pathology.

The click-rate induced facilitation of the acoustic reflex thresholds¹² is known to be affected by the aging process.¹³ When acoustic reflex measures are elicited with frequency-specific stimuli for detection of retrocochlear pathology, the use of a single-frequency criterion, without consideration of other frequencies, is known to yield a high rate of false negatives.¹¹

Click stimuli have a broader frequency spectrum and thus may be more efficient in detection of retrocochlear pathology. Johnsen and Terkildsen¹⁴ reported that the use of clicks allows better definition of acoustic reflex thresholds than white-noise stimuli. Thus, click-activated acoustic measures have the potential to enhance clinical diagnosis.

Moller⁵ used trains of band-pass filtered pulses to activate the acoustic reflex. The center frequencies of the bandpass filtered pulses were 525 Hz and 1450 Hz, and the bandwidth was 100 Hz. The repetition rates for the pulses varied from 10 pulses to 50 pulses per second. The frequency of the probe tone was 800 Hz. Moller⁵ measured the impedance change 20 msecs after the stimuli were switched off using an X-Y recorder. He reported greater sensitivity of the acoustic reflex for ipsilateral stimulation than for contralateral stimulation. The total number of subjects used in the study was not specified.

For adequate use of click-evoked acoustic reflex measures in clinical investigations, the differences in ipsilateral and contralateral mode in a group of normal individuals need to be documented. Such differences can also be helpful in improving our understanding of any functional differences in the ipsilateral and contralateral acoustic reflex pathways.

Purpose of the Investigation

The purpose of this study was to document the effect of activation mode (ipsi- versus contra-lateral) on the click-evoked acoustic reflex thresholds in normal individuals. The investigation was also designed to improve the methodological concerns raised in previous studies.⁸ During the measurement of the ipsilateral acoustic reflex, the probe tone and the reflex-activating stimuli are presented simultaneously to the same ear. Thus, the two stimuli can interact, causing stimulus artifacts.⁴

A multiplexed stimulus approach, in which the probe and the reflex activating stimuli are presented alternately, minimizes the possibility of the interaction of the two stimuli.¹⁵ The multiplexed stimulus approach relies on the fact that the off latency of the acoustic reflex is fairly long. Thus, the reflex can be measured after the reflex-activating stimulus is turned “off.” The probe tone can be introduced during the period when the reflex-activating stimulus is off, to measure the reflex-induced change in middle ear admittance. Thus, simultaneous presentation of the probe and the reflex-activating stimuli can be avoided.

Study Methods

Participants. A total of 14 women ages 19-32 years participated in the study. They had no known neurological abnormalities, normal tympanometric findings, and presence of acoustic reflexes in both ipsilateral and contralateral modes and auditory sensitivity within normal limits. Their auditory sensitivity was within 20 dBHL for the frequencies from 250 to 8000 Hz.

Procedures. The reflex recording was achieved with the commercially available Grason-Stadler GSI-33 (Version 2) middle ear analyzer, using previously described procedures.^5,6,12,13 The GSI-33 system offers the option of the multiplexed stimulus approach for both the ipsilateral and contralateral reflex measurements. The envelope for the multiplexed stimulus is 115 ms. Within this period, the clicks are presented for 44 ms and the probe is presented for 53 ms (the clicks are off during this time period). The total rise and fall time of the envelope is 18 ms.

A schematic illustration of the multiplexed stimulus approach has been presented previously by the author.¹² During contralateral acoustic reflex measures, direct interactions of the probe and the activating stimuli are not possible, since the probe is presented to the test ear and the reflex activating stimuli are presented to the contralateral ear. However, for adequate comparisons of acoustic reflex thresholds in the ipsi- and contra-lateral modes, it is necessary to keep the stimuli similar in both the modes. Therefore, the multiplexed stimuli were used for both the ipsi- and contra-lateral measurements; during both measurements, the reflex-activating clicks and the probes were presented alternately.

The reflex was activated using clicks presented at the rate of 100/sec. The polarity of the click was condensation and the duration of the click was 100 microseconds. The frequency range of the ipsilaterally delivered clicks in the GSI-33 system is 50 to 4000 Hz and that of the contralaterally delivered clicks is 50 to 3600 Hz.

For ipsilateral measurements, the clicks in the GSI-33 system are delivered through a loudspeaker located in a compact probe box. The probe box is coupled to the ear canal through long tubes attached to an eartip (probe-cuff). The eartip holds the probe in place and hermetically seals the ear canal. The probe box also has an additional loudspeaker, a microphone, and a pressure transducer. The additional loudspeaker delivers the probe tone to the ear canal and the microphone monitors the intensity of the probe tone in the ear canal during both the ipsilateral and contralateral measures. The pressure transducer allows variation of the pressure in the ear canal so that the pressure can be maintained at the point of peak middle ear admittance. The delivery of contralateral stimuli is achieved through a button transducer that is coupled to the ear canal by the eartip, similar to that used during ipsilateral measures.

Acoustic reflex thresholds were established for the left ear of each subject using ipsilateral and contralateral activators. The frequency of the probe tone was 226 Hz and the intensity was 85 dBSPL based on measurements in an ANSI HA¹ coupler. Each measurement was made over a period of 1.5 secs.

The graphic display of acoustic reflex tracings along with the stimulus onset and termination markers was visually monitored for any apparent stimulus artifacts. The lowest intensity value at which a minimum of 0.02 ml change in admittance was apparent on at least two of three trials was considered to be the reflex threshold. The GSI-33 provides the admittance values based on the maximum change in admittance from the baseline admittance, recorded within the time frame of measurement (1.5 secs). For a 226 Hz probe, the admittance is reported in ml units because the admittance at this probe frequency is dominated by compliance. The compliance is calibrated with respect to the compliance of an equivalent volume of air in ml.

Reflex thresholds were determined by increasing or decreasing click levels in 5 dB steps. The subjects were instructed not to move, swallow, or talk during data collection. If subject movements occurred during data collection, the relevant data were discarded. All the data were collected in a quiet room.

Statistical analyses were performed using commercially available statistical software. Repeated measure Analyses of Variance were performed to determine any differences in acoustic reflex thresholds in the ipsilateral and contralateral mode.

Results

The mean, standard deviations, and range of the ipsilateral and contralateral acoustic reflex thresholds are presented in Figure 1. The analyses revealed that the acoustic reflex thresholds in the contralateral mode were significantly [F (1,13) = 11.48; p < 0.0049] higher (worse) than those obtained in the ipsilateral mode. The mean difference between ipsilateral (86.79 dB peSPL) and contralateral (98.21 dB peSPL) acoustic reflex thresholds was 11.42 dB.

Discussion

These results revealed that acoustic reflex thresholds are significantly better (lower) in the ipsilateral mode. These findings are in agreement with other reports of acoustic reflex measures for tonal and broadband noise activators.²-6 For click stimuli, the mean difference between the ipsilateral and contralateral acoustic reflex thresholds is 11.50 dB.

In the current investigation, there was a slight difference in the click-spectrum in the ipsilateral and contralateral modes. The frequency range of the ipsilaterally delivered clicks was 50 to 4000 Hz, and that of the contralaterally delivered clicks was 50 to 3600 Hz. However, this spectrum difference is likely to cause minimal differences, if any, since the reflex activation is fairly weak at higher frequencies. At 4000 Hz, the acoustic reflex is often absent in normal-hearing individuals.

Differences in Ipsilateral and Contralateral Reflex Pathways

The physiology of the human acoustic reflex is unknown due to experimental limitations. In animals, interspecies differences have been reported.¹⁶ However, the human acoustic reflex pathway can be predicted, with caution, from animal studies.

Although the acoustic reflex is activated bilaterally upon stimulation to one ear, the ipsilateral and contralateral acoustic reflex pathways are somewhat different. During the elicitation of the ipsilateral acoustic reflex, the reflex-activating stimulus travels through the outer and middle ear to the cochlea. The neural impulses then travel from the cochlea, through the auditory nerve, to the ventral cochlear nucleus, and from the ventral cochlear nucleus to the trapezoid bodies or to the medial superior olive.^17,18 A message is then relayed to the stapedial motoneurons,¹⁹ which travels through the motor nerve fibers to the stapedius muscle.

The changes in the middle ear admittance induced by the contraction of the stapedius muscles are measured in the same ear. During the contralateral measures, the reflex activating stimuli are presented to the contralateral ear. The stimuli travel through the contralateral outer and middle ear to the contralateral cochlea. From there, the neural impulses travel to the contralateral ventral cochlear nucleus and then to the medial superior olive, possibly through the trapezoid bodies.

From the superior olive, a message is then relayed to the ipsilateral stapedial motoneurons, which travels through the ipsilateral motor nerve fibers to the stapedius muscle. The muscle contracts, and the changes in middle ear admittance due to this contraction are measured by the probe placed in the ipsilateral ear.

Vacher et al²⁰ demonstrated that the cell bodies of stapedius motoneurons, with different response lateralization, tend to have different locations in the brainstem. Kobler et al²¹ suggested that the innervations of the crossed and uncrossed stapedius acoustic reflexes in cats are provided by a different mix of interneurons.

Kobler et al²² established four different categories of stapedius motoneurons in cats on the basis of their response laterality. The first group of neurons responded to stimuli delivered to either ear (50%). The second group responded only to ipsilateral stimuli (32%). The third group of stapedial motoneurons responded only to contralateral stimuli (12%), and the fourth group responded only to binaural stimuli. This investigation suggests that the total percentage of activated stapedial motoneurons is about 20% higher during ipsilateral activation than during contralateral activation. Thus, better thresholds for ipsilateral reflex measures can be expected.

The findings of better ipsilateral acoustic reflex thresholds are supported by other related reports. Evidence from cats shows that the ipsilateral reflex may provide substantially more attenuation of sound transmission than the contralateral reflex. In cats, EMG activity of the stapedius muscles on ipsilateral stimulation is 2 to 3 times greater than the EMG activity following contralateral stimulation.²³

Functional Significance of Difference in Ipsilateral and Contralateral Reflex Thresholds

Kobler et al²² suggested that the recruitment order in the stapedius motoneuron pool can change as a function of the free-field location and spectral composition of sounds, which elicit the acoustic reflex. Thus, the differences in ipsilateral and contralateral acoustic reflex thresholds may have some functional significance in localization of loud sounds.

Lawrence²⁴ suggested that the acoustic reflex might enhance sound localization by asymmetrical shifts in phase and intensity. Iguchi et al²⁵ reported that, when the sound source is placed laterally near an ear, the amplitude of the acoustic reflex is higher in that ear than in the contralateral ear. Such differences are likely to be helpful in maintaining the sense of sound direction for loud stimuli.

Clinical Consideration

The current investigation confirms the need for considering the normative differences in ipsilateral and contralateral click-evoked acoustic reflex thresholds when considering reflex activation during ototacoustic emission and ABR measures²⁶ and when using the reflex measures in otoneurologic diagnosis.

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Correspondence can be addressed to HR or Vishakha W. Rawool, PhD, at .