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Pitfall

Madell et al., Pediatric Audiology: Diagnosis, Technology, and Management, 3rd Ed. (ISBN 978-1-62623-401-7), copyright © 2019 Thieme Medical Publishers. All rights reserved. Usage subject to terms and conditions of license.

A sleeping baby is a ticking time bomb, waiting to go o. The concept of using a xed number of sweeps wastes time when the

response is large and recording conditions are good, whereas

near threshold and in poorer recording conditions, a xedsweeps approach is almost guaranteed to yield scientically

questionable results. Our job just got harder—we must invest clinical test time to maximize the information we gather. That means developing an interactive test strategy that is focused on satisfying waveform CR or RA criteria in the minimum time. That in turn means continual quick thinking and good judgment, basing our strategy on the assumption that the baby will wake up one minute from now.

13.4.5 Cross-Hearing

Just as in conventional behavioral audiometry, cross-hearing can occur in ABR tests. The interaural attenuation in newborns is some 10 to 30 dB greater than in adults,23 and this works in our favor, reducing the need for masking. If a BC response is

present at 15 dB eHL or less, or if the right–left BC ABR thresholds

are within less than 20 dB of one another, masking is probably unnecessary.7 Fig. 13.6 is such an example. If a response could be crossed, there are a number of methods we can employ to resolve the issue. One is to record a two-channel ABR. The recording channel yielding the larger and earlier latency wave V is likely to be on the side of the ear generating the response,24 and if this is the stimulated side, masking is not needed. Similarly, the

recording channel exhibiting a wave I (a near-ﬁeld response for

the mastoid electrode) will be on the side of the ear generating the response. Recent evidence25 suggests that the superior neural synchrony oered by chirps over tone bursts increases the proportion of cases in which wave I is seen at stimulus levels close

to threshold. When these methods fail to conﬁrm that the ABR

originates from the stimulated side, masking should be applied to determine the true ABR threshold of the worse ear. The level of noise to apply to the nontest ear is dependent on a number of factors; we have developed a masking noise calculator26 to simplify the process.

13.4.6 Estimating the Audiogram

The ABR threshold, in dB nHL, is not the same as the estimated hearing threshold, in dB eHL; two issues should be considered

when applying any conversion. The ﬁrst is the average level at

which an ABR is normally seen above the patient’s audiogram.

This is frequency dependent, with greater dierences seen at

lower frequencies because of poorer neural synchrony. It is also dependent on the quality of the recording conditions and

Fig. 13.6 Air and bone conduction ABR waveforms in a 4-week-old baby, tested at 4 kHz. Upper panel: AC ABR threshold is “=50 dB nHL”;

lower panel: BC ABR threshold is “≤ 10 dB nHL.” For this 4-week-old

baby and for the transducers and stimulus frequency used, dB nHL = dB eHL for both AC and BC. Masking was not needed for BC since a response was recorded at a level that was too low to be from the opposite ear, after accounting for a presumed BC interaural attenua tion of 20 dB.

waveform interpretation and, for tone burst stimuli and clicks, assumes that the stimuli are 2:1:2-cycle and calibrated to levels

given in ISO 389-6. It includes an element representing the

maturation of the ABR threshold with age.

related transducer oset, applicable to insert and BC transducers

as previously discussed. Table 13.4 is taken from the English NHSP guidance and combines both elements, providing appendices with details of their derivation. The corrections should be a

dded to the ABR threshold in dB nHL to produce an estimated

hearing level in dB eHL.7 To our thinking, this approach is both

technically and clinically superior to one in which dierent stimulus levels are quoted for “satisfactory hearing” or “minimum levels” across frequencies. Audiologists like audiograms; dB eHL

provides them.

The second is an age-

II Diagnosing Hearing Disorders in Infants and Children

Table 13.4 Corrections to be added to ABR thresholds in dB nHL to estimate the hearing level (dB eHL) in babies up to 12 weeks corrected age

Tone burst ABR Chirp ABR

Frequency (Hz) 500 1,000 2,000 4,000 500 1,000 2,000 4,000 Insert phones –15 –10 –5 0 –10 –5 0 5 Supra-aural earphones –20 –15 –10 –10 –15 –10 –5 –5 Bone conductor 5 5 –5 0 10 10 0 5

Corrections for older children and for clicks are available from the English NHSP guidance.

13.4.7 Reporting, Accuracy, and

Condence Limits

ABR results, reported in either stimulus levels (dB nHL) or estimated hearing level (dB eHL), should use a standard and agreed nomenclature. Where no response is evident at any st imulus level,

the result should be expressed as “> X,” where X is the maximum level at which the formal “response absent” criterion has been satisﬁed. Where the ABR has been deﬁned with a CR at level X, and an RA at a level no lower than X – 10 dB, the ABR threshold should be reported as “= X.” When RA has not been demonstrated,

but a CR is evident at level X, the result should be reported as

“≤ X.” Note that results using the ≤ format could be within the

normal range, and testers must acknowledge the importance of identifying RA when the threshold is raised. The use of phrases

such as “responses were seen down to . . .” is discouraged. In Fig.

13.6 the AC result is = 50 dB nHL, and the BC result is ≤ 10 dB

nHL. We recommend that responses not meeting formal CR or RA criteria should be excluded from any diagnostic report; any that are mentioned, must be expressed with appropriate caution.

An example might be “a possible but uncertain response was recorded at Y dB nHL, but this should not be relied upon.” An ABR report should include an estimate of the likely conﬁdence intervals. The 5 to 95% range has been estimated at around ±15 dB for

requency-speciﬁc stimuli but much greater for click stimuli.

All programs should be designed to include an integrated

system of independent peer review and clinical audit of their

service. The British Society of Audiology has deﬁned what this

should involve for ABR services.

7,2 7

13.5 Neurologic ABR/CM Testing

In neurologic testing, we have a dierent priority for threshold

estimation. We are less interested in determining whether a response is present or absent but whether the response characteristics provide any evidence of pathology in the auditory neural pathways. Here, we analyze the recorded waveform, often evoked at a single stimulus level, in terms of the latency or amplitude of characteristic peaks. T he ABR is thought to mature fully by the age of 2 years,29 allowing comparison to adult reference data. Below this age, incomplete neural myelination results in longer latencies

in otherwise neurologically intact patients. Limited age-speciﬁc

reference data does exist.30 or interaural measurements may be made. The stimulus is a 100-µs click of either alternating or rarefaction polarity (opinion continues to be divided) at typically

80 dB nHL. The pattern of abnormal ABR can vary across and

within pathologies, depending on the nature, site, and severity. For example, hydrocephalus can mildly attenuate and delay wave V only or, when severe, can obliterate all but ABR wave I.

is typically characterized by an absent or severely

ANSD abnormal ABR in the presence of normal cochlear hair cell function according to recorded OAE or CM. Unlike the ABR, the CM waveform inverts as the stimulus polarity is inverted; therefore, separate rarefaction and condensation clicks are used and their waveforms compared. Like the OAE, the CM is not neurogenic and does not adapt at high stimulus rates. The optimum CM test,32 therefore, uses a very fast rate (typically 89/s) and a 10-ms recording window. The spectrum of the response also allows the use of

a high-pass ﬁlter of 100 to 300 Hz, which attenuates almost all

patient myogenic noise, permitting a strict (±3 µV) artifact rejection level to be applied for fast, low-noise waveform acquisition. In cases where a possible CM is seen, a stimulus artifact should be ruled out by clamping the insert tube and by making another recording. A genuine CM should disappear; if not, the apparent CM must be discounted as an artifact. Both the CM and click ABR recordings should be acquired at the same click stimulus level,

typically 80 dB nHL but never above 85 dB nHL in a baby unless

ANSD has been excluded. Fig. 13.7 illustrates ANSD in a well baby

with no risk factors, born at 38 weeks. The baby was referred by

the OAE screen even though tympanometry and, later, CM testing proved to be normal. In the UK, well babies are screened by OAE, so this ANSD case would have been missed had OAE been present. Diagnostic testing revealed the ABR was absent and CM was pres-

ent bilaterally. Imaging revealed no identiﬁable auditory nerves.

13.6 Threshold ASSR Testing

The term auditory steady-state response is an umbrella term

that refers to responses that originate from dierent parts of the

auditory pathway depending on the stimulus parameters. The set of parameters that are used during the ASSR will depend on the clinical question being asked and the patient being tested. Table 13.5 gives a summary of these relationships. The sources are not exclusive, and there may be multiple parts of the auditory pathway contributing to the response.

The stimulus is typically a pure tone, of an audiometric frequency, which is modulated in some way at a speciﬁc rate. In contrast to the ABR, where the responses are averaged and visually inspected in the time domain, in the ASSR the responses to each

“stimulus cycle” are collated sequentially and converted to their

frequency components. The activity at the stimulus modulation frequency (and its harmonics) is, then, compared to other frequencies in the spectrum to determine the presence or absence of a physiologic response. Visual analysis of the time waveform is not available to the tester; the devices, instead, give probability values regarding the likelihood that the response is genuine. These values

currently vary with device, and dierent algorithms are used to

reach these values.

142

Fig. 13.7 Click ABR and CM results in a baby with ANSD. Note the

“mirror-image” CM, which disappears when the insert tube is clamped,

conrming it is not stimulus artifact.

As we search for ways to increase the speed of testing, particularly in newborns, the ASSR is attractive. Not only can we successfully and simultaneously test multiple frequencies within a single ear; simultaneous dichotic testing is possible and commonly used.

However, there are limitations to this testing, and the eciency of

the test is not in proportion to the number of test frequencies.33

The eciency is limited by certain factors that are inuenced by

the stimulus and recording parameters. For example, in the pres-

ence of 500-Hz stimuli, the threshold of 2,000-Hz and 4,000-Hz may be signiﬁcantly raised.34 If it is not required to answer the

clinical question, there is an argument to exclude it from the test.

Interactions that have been observed in dierent patient groups

are summarized in Table 13.6.

Table 13.5 Parallels of ASSRs at dierent modulation rates to other

auditory electrophysiologic responses

Modulation rate

80–100 Hz Asleep ABR wave V/SN 40 Hz Awake MLR < 2 Hz Awake CAEP

Abbreviations: ABR, auditory brainstem response; CAEP, cortical auditory evoked potential; MLR, middle-latency response; SN 10 ms (following wave V).

Optimum patient state

Equivalent transient response

, slow negative wave at

Table 13.6 ASSR paradigms where amplitudes can be reduced in the presence of simultaneous stimuli presented at moderate intensities

Adults

40 Hz

Multiple within one ear Yes Dichotic presentation Yes

On this journey toward a more accurate assessment, a range of stimuli have been developed. In the early days of ASSRs, amplitude-modulated tones were used as stimuli;

it was identiﬁed that the extent and type of modulation can dramatically inuence the amplitude of the response.36 The

range of stimuli available to the tester now includes exponential envelopes37 and modulated noise.38 Of particular note is the chirp stimulus. As for the ABR, the chirp has been found to successfully evoke a larger response than more conventional

stimuli.

The relationship with behavioral responses are similar to those of other electrophysiologic measures that originate at the same points on the auditory pathway. As an example, ASSRs to

80 to 100-Hz modulated tones, thought to originate largely from

the brainstem, have been found in hearing impaired listeners

to have osets in the range 5 ± 8 dB to 17 ± 14 dB

13.7). The oset size and range varies with stimulus, transducer,

and age of patient. It also decreases with increasing degree of hearing loss.

Like so many other auditory electrophysiological responses, the ASSR is susceptible to artifactual interference. The risks are arguably greater for this particular methodology, as the responses are recorded at the same time as stimulus presence, so there is no opportunity to isolate the response using delay analysis. Devices are more resilient to this than they were in the past, but the tester should be aware of the risks, and if there is uncertainty, blocked stimulus runs are particularly valuable in distinguishing physiologic from artifactual responses.

Although the ASSR is widely used for a wide range of patients from newborns to adults, this test has its limitations, so it is recommended that outcomes of ASSR testing be considered only within the context of the broader test battery.

Table 13.7 Corrections to be added to ASSR thresholds in dB nHL to estimate the hearing level (dB eHL) in babies up to 12 weeks corrected age, and with thresholds > 30 dB nHL

Frequency (Hz) 500 1,000 2,000 4,000 Insert phones –20 –20 –15 –15 Supra-aural earphones –25 –25 –20 –25 Bone conductor Not available

Source: Based on Stevens et al.

Adults

80–100 Hz

Yes

Infants

80–110 Hz

Yes

however,

34,40

(Table

II Diagnosing Hearing Disorders in Infants and Children

Discussion Questions

1. How can behavioral hearing thresholds be estimated from

ABR and ASSR thresholds?

2. What is the eect of age on the ease and precision of ABR and

ASSR testing, and what are the consequences of this for the design of hearing screening programs?

3. Chirp stimuli can oer reduced test times and/or improved

test quality over tone burst stimuli. Through what mechanism is this achieved?

4. What is weighted (Bayesian) averaging, and what benet does

this bring over conventional averaging?

5. What choices are available to deal with possible cross-hearing?

6. Some ABR systems oer objective measurements. How

can they be used to inform test strategy and waveform interpretation?

7. What are the key results that describe ANSD?

References

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[2] Elberling C, Wahlgreen O. Estimation of auditory brainstem response, ABR, by

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[3] Don M, Elberling C. Evaluating residual background noise in human auditory

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[4] Stapells D. Frequency-speciﬁc ABR and ASSR threshold assessment in young

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[5] Sutton G, Lightfoot G. Guidance for Auditory Brainstem Response Testing in

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[6] Elberling C, Don M. Quality estimation of averaged auditory brainstem respons-

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[7] Stevens J, Sutton G, Wood S. Guidelines for the Early Audiological Assessment

and Management of Babies Referred from the Newborn Hearing Screening Pro-

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[8] Lightfoot G, Stevens J. Eects of artefact rejection and Bayesian weighted averag-

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[13] International Electrotechnical Commission. IEC 60645–3:2007. Electroacous-

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Otorhinolaryngol 2013;77(9):1555–1560

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and estimation of hearing threshold using frequency-speciﬁc chirp and tone pip stimuli in newborns: Findings at 0.5 and 2 kHz. Int J Audiol 2015;54(10):745–750

[19] Hatton J, Hyde M, Stapells D. BC Early Hearing Program: Audiology Assessment

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Hyde M. Ontario Infant Hearing Program: Audiologic Assessment Protocol, Ver-

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[23] Small SA, Stapells DR. Maturation of bone conduction multiple auditory steady-

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[36] Cohen LT, Rickards FW, Clark GM. A comparison of steady-state evoked

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144

14 Clinical Measurement and Application of Cortical Auditory Evoked Responses

14 Clinical Measurement and Application of Cortical Auditory

Evoked Responses

James W. Hall III, Zeina Zayat, and Maryam Aghamolaei

Summary

Clinical measurement and application of cortical auditory evoked responses plays an important role in the diagnosis of hearing loss in infants and young children. The auditory middle latency response and auditory late responses can be recorded with clinical devices typically used for measurement of the auditory brainstem response. Research evidence clearly con-

ﬁrms the value of these cortical auditory evoked responses in

the evaluation of varied pediatric patient populations, including auditory processing disorders, language and learning disorders, auditory spectrum disorder, and auditory neuropathy spectrum disorder. Recent research also shows that cortical auditory evoked responses can also be applied in objective documentation

of beneﬁts from intervention with ampliﬁcation and cochlear

implantation. As a cognitive measure, the P300 response contributes rather uniquely to assessment of high-level auditory function involving memory and attention. Cortical auditory evoked responses are now among the objective procedures within the modern test battery that serve in the implementation of the cross-check principle in pediatric hearing assessment. In this chapter we provide practical information on clinical measurement and analysis of the auditory middle latency response, the auditory late response, and the P300 response.

amplitude, auditory middle latency response, auditory late response, auditory processing disorders, latency, primary auditory cortex, P300 response

Research reported in thousands of peer-reviewed publica-

•

tions documents clinical applications of cortical auditory evoked responses in pediatric populations.

Cortical auditory evoked responses oer a clinically feasible

•

and evidence-based option for objective assessment of central ner vous system func tioning in infants and young children. The auditory middle latency response and the auditory late

•

response can typically be recorded with the same equipment used for auditory brainstem response recordings. Clinical practice guidelines support the application of cortical

•

auditory evoked responses in the assessment of children undergoing diagnosis for (central) auditory processing disorders. Cortical auditory evoked responses can play an important

•

role in the diagnosis and management of auditory neuropathy spectrum disorder.

14.1 Cortical Auditory Responses

Cortical auditory evoked responses are not new. The ﬁrst

reports describing measurement of electrophysiologic activity in response to sound stimulation date back to the late 1930s,1 and until the auditory brainstem response (ABR) was discovered in 1970, responses arising from the auditory cortex were investigated and applied clinically as a tool for estimating auditory thresholds in young children. discovered the auditory middle latency response (AMLR), which

Goldstein and colleagues at the University of Wisconsin soon

applied in the assessment of auditory thresholds in young children, including newborn infants.

With the emergence in the mid-1970s of the use of ABR as a

clinical tool for pediatric auditory assessment, clinical use of the AMLR and auditory latency response (ALR) quickly diminished. However, within a decade the need for an electrophysiologic measure of higher-level auditory function began to be appreciated in clinical audiology. mation of auditory threshold and detection of brainstem auditory dysfunction (see Chapter 13), but it provides no information on higher-level auditory function.

2,3

The ABR was and remains valuable for esti-

2,3

Less than 20 years later, Geisler

14.2 Confusing Terminology

Terminology for the description of auditory evoked responses is rather inconsi stent, ambiguous, conf using, arbitrary, and espec ially troublesome with cortical responses. A good example of this statement is the variety of terms used for the cortical auditory evoked response refer red to here as the AL R. In the years since its discovery,

terms for describing the response have included “vertex response,” “vertex potential,” “auditory cortical response (ACR),” “auditory evoked potential (AEP),” “averaged electroencephalic response (AER),” and “slow averaged evoked potential” (or “response”), “cortical evoked response audiometry (ERA),” “electroencephalic response (EER),” “electroencephalic audiometry (ERA),” and, most recently, “cortical auditory evoked potential (CAEP).”

Two general approaches are taken to label or describe responses that occur later in time than the ABR. One approach is based on latency and the temporal sequence of components. With this schema, cortical auditory evoked components are described in relative terms on the basis of their latency. The auditory middle latency response is so named because it follows the ABR and it precedes the auditory late responses. The auditory late responses

are characterized by even longer latencies. The term “P300 response” refers to its typical latency of approximately 300 ms.

At least two problems immediately arise with the temporal sequence approach for classifying or labeling auditory evoked responses. First, there may be additional auditory evoked response components within a general latency region under certain stimulus conditions and subject states. The literature includes papers

145

II Diagnosing Hearing Disorders in Infants and Children

describing dozens of speciﬁc components or waves, all within the latency region of 50 to 500 milliseconds. Also, developmental factors in young children exert pronounced inuences on the latency

of auditory evoked responses and even their presence or absence. For example, the AMLR in adults consists of prominent positive

waves within the 25-ms time frame (the Pa component) and the 50-ms region (referred to as the Pb or P50 component). However, for infants and young children the Pb or 50-ms component actu-

ally occurs much later, often far beyond 100 ms and well within the conventional time frame for the auditory late response. Also, the major ALR components are not observed in recordings from infants and young children.

Another approach for nomenclature is in reference to auditory

anatomy. An obvious example is the now commonly used phrase

“cortical auditory evoked potential (CAEP)” (frequently used in

other chapters within this volume). Several problems are also associated with this strategy. First, the rather vague and nonspe-

ciﬁc term encompasses a spectrum of responses arising from the

auditory cortex, including the AMLR, the P300 response, the MMN response, the sustained potential, and up to six components that contribute to the N1 wave alone, depending on the site of the recording electrode. The other problem with using the phrase is

inconsistency in use of the word “potential” alongside accepted

terminology for the auditory brainstem response and auditory middle latency response. The latter two responses are not referred to as potentials.

There is one example of consistency in terminology for auditory evoked responses later in latency than ABR. Nomenclature for describing waveforms according to positive and negative peaks as recorded with electrodes located at the vertex or on the scalp over the auditory cortex is still used today. All auditory evoked response waveforms recorded from cortical regions include components labeled with P for positive and N for negative.

diagnostic assessment of infants and children is entirely in compliance with the cross-check principle, which Jerger and Hayes

proclaimed over 40 years ago, stating clearly: “We have found

that simply observing the auditory behavior of children does not always yield an accurate description of hearing loss. In our own experience, we have seen too many children at all levels of functioning who have been misdiagnosed and mismanaged on

the basis of behavioral results alone.” responses are a viable, and really the only, option for conﬁrming or “cross-checking” ﬁndings of behavioral hearing assessment in

children.

5,6

7[614]

Cortical auditory evoked

Pearl

Measurement of the AMLR and ALR in some children is consistent with the cross-check principle in pediatric audiology.

Even before the discovery of the ABR, the disadvantages of late

auditory evoked responses as a tool for auditory threshold estima-

tion in young or dicult-to-test children were well appreciated.

uiet patient state with minimal movement interference is

A q

required for conﬁdent detection of late responses. Unfortunately,

cortical evoked responses are suppressed or eliminated with

sedation or anesthesia, and even natural sleep markedly aects

reliable measurement of cortical responses. Nonetheless, as summarized in this chapter, recent research suggests that cortical auditory evoked responses can play a role in the assessment and management of infant hearing loss.

14.4 Auditory Middle Latency

14.3 Rationale for Clinical

Application

Like other objective measures of auditory function, cortical auditory evoked responses are not dependent on a behavioral

response to sound stimulation. Speciﬁcally, valid recordings

of cortical auditory evoked responses are possible without the inuence of listener (patient) variables that may confound traditional behavioral tests, such as motivation, fatigue, cognition, attention, motor function, and language. Admittedly, cortical evoked responses do not share some of the advantages of other objective auditory tests such as aural immittance measures and otoacoustic emissions (OAEs), including brief test time, simplicity in administration, independence of patient state of arousal,

and the eects of sedation and anesthesia.

Cortical auditory evoked responses, however, do oer clinical

advantages not found in these other objective auditory tests. Aural immittance measurements and OAEs are not tests of hearing. They provide important information on function of the peripheral auditory system and, if contralateral acoustic reexes are measured, portions of the auditory brainstem. In contrast, cortical auditory evoked responses yield electrophysiologic information on function of the highest levels of the auditory system. Inclusion of cortical auditory evoked responses whenever possible into

5,6

Response (AMLR)

14.4.1 Measurement

Measurement of the AMLR does not need any speciﬁc equipment.

That is, the response can be easily recorded with a clinical ABR system using an appropriate protocol. The reader is referred to the recent textbook by one of us (Hall)3 for an evidence-based test protocol for clinical measurement of AMLR. It is important

to note that some parameters and values need to be modiﬁed for

consistent detection of the Pb component. The same protocol can be used in both adult and pediatric populations, with adjustments

in speciﬁc parameters for children younger than 10 years old. The

important topic of age as a factor in AMLR measurement is dis-

cussed later. Selected parameters do not aect the detectability

of the response. For example, one could use either a supra-aural or an insert earphone in recording AMLR, although insert phones

oer some advantages, especially in pediatric assessments.

Similarly, stimulus polarity (rarefaction, condensation, or alternating) is not a critical factor in recording AMLR.

However, some other parameters directly aect the amplitude,

latency, and morphology of AMLR and must be selected carefully to ensure consistent detection of AMLR. Both click and tone burst stimuli can be used to evoke AMLR for neurodiagnostic purposes,

146

14 Clinical Measurement and Application of Cortical Auditory Evoked Responses

but only tone burst stimuli can be used for frequency-speciﬁc

estimation of hearing thresholds. In general, longer-duration

tone burst stimuli (> 10 ms) with abrupt rise/fall times are more eective and preferred in evoking AMLR, especially for recording

the Pb component. For both clinical applications of AMLR, stimuli are presented monaurally. Binaural AMLR measurement does not have any apparent clinical indication.

The eect of stimulus rate on AMLR components interacts with the eects of age, drugs, and central nervous system (CNS) pathology. For adults, rates between 8/s to 11/s have been successfully used in recording AMLR. Rates below 5/s are more appropriate

for AMLR measurement in young children, and they are certainly

suitable for adults as well. Rates as low as 0.5/s to 1/s are optimal

for recording the AMLR in newborn infants and also for consis-

tently recording and conﬁdently detecting the Pb wave in both

adult and children.

Usually about 1,000 stimuli are presented for AMLR recording, but depending on the signal-to-noise ratio, a far smaller number of stimuli might be required.

2,3

Stimulus level at about 70 dB normal

hearing level (nHL) is appropriate for neurodiagnostic purposes, in both adults and children. Higher intensity levels should be avoided, as they can evoke myogenic postauricular muscle (PAM) artifact, which may obscure true AMLR components. In addition to lowering stimulus intensity level, the PAM response is usually diminished if a patient’s neck muscles are in a relaxed position. Use of a noncephalic inverting electrode on the nape of the neck is

another simple and eective strategy for minimizing the negative

impact of PAM artifact on AMLR recordings.

Filtering, especially selection of the high-pass ﬁlter cuto

frequency, is one of the most important parameters in AMLR

measurement, as it removes the eects of low-frequency encephalographic (EEG) activity on the response. The ﬁlter setting should

be selected carefully based on the purpose of AMLR recording. A

bandpass ﬁlter of 10 to 200 Hz is appropriate for reliably recording the Na and Pa components; however, a lower high-pass ﬁlter

setting, such as 1 or 0.1 Hz, is necessary for consistent detection of the Pb component. For combined recording of ABR and AMLR with

Na and Pa components, a higher low-pass ﬁlter, such as 10 to 1,500 Hz, is required. Restricted band-pass ﬁltering, such as 30 to 100 Hz, must be avoided, as it may introduce a ﬁlter artifact in the latency

range of Pa, even when the actual response is not present.

2,3

Electrode sites and the number of channels in AMLR record-

ing are deﬁned based on the purpose of measurement. For

estimation of hearing sensitivity, single-channel recording with a noninverting electrode in the midline (either Fz or Cz) and a linked earlobe (Ai/Ac) or a noncephalic inverting electrode is appropriate. However, for neurodiagnostic measurement of AMLR, a two-channel recording arrangement is necessary with an

electrode located on each hemisphere at sites such as C3 and C4 or C5 and C6. Hemispheric noninverting electrodes are required to

make comparisons between the two auditory cortices.

2,3

14.4.2 Analysis and Interpretation

A typical AMLR waveform is shown in Fig. 14.1. The ﬁrst step in analysis of an AMLR waveform is, of course, determining the presence or absence of a reliable response. Two criteria are often used for concluding presence or absence of the AMLR.3

Fig. 14.1 Typical auditory middle latency response waveform showing major components. (Courtesy of Hall JW III. eHandbook of Auditory Evoked Responses. New York, NY: Kindle Direct Publishing; 2015)

A response is present if (1) there is electrical activity below or

above a baseline deﬁned by ABR, corresponding to Na and Pa

components, respectively, and (2) the typical morphology of an AMLR waveform is observed, including a negative trough (Na) followed by a positive Pa component.

Response reliability is an important factor that can help the

clinician in conﬁdent analysis of the AMLR. Reliability should always be conﬁrmed, as it is for the ABR. However, in contrast to

the ABR, analysis and interpretation of the AMLR is not always straightforward in clinical settings. The challenges are mostly due to certain methodologic and nonpathologic factors that can alter the response. In other words, while the presence of the response provides valuable information about the integrity of part of the central auditory nervous system, the absence or deterioration of the AMLR is not necessarily an indication of hearing loss or CNS dysfunction. One must rule out every possible methodologic explanation before making any conclusions about the auditory functional status of the subject.

The other concern in analysis of AMLR is whether or not the

recorded components are neurogenic.

In fact, even the presence

of the AMLR needs to be conﬁrmed, as there are two highly reliable

artifacts that occur in the time range of the Na and Pa components and, therefore, can be mistaken for the actual AMLR components. We have already mentioned the most troublesome artifact that must be ruled out: the myogenic PAM artifact. The other one is the

ﬁlter artifact, which is caused by restricted ﬁltering. These two

artifacts and suggested parameters and test strategies to avoid them were reviewed in the preceding section.

147

II Diagnosing Hearing Disorders in Infants and Children

Analysis of AMLR is mostly based on the calculation of latency and amplitude, especially amplitude. In contrast to the strategy for ABR analysis, for the AMLR there is more reliance on response amplitude rather than latency. Intra- and intersubject variability of amplitude is lower than for latency, and it seems to be more

aected by CNS dysfunctions. In AMLR analysis, latency is not

as informative as it is in earlier responses. Therefore, clinical information, for the most part, is derived from amplitude values of AMLR’s major components, including Na, Pa, and Pb.

The most common and clinically feasible strategy is simultaneously recording the AMLR using at least two noninverting electrodes on the hemispheres (such as C3 over the left hemisphere

and C4 over the right hemisphere). Also, if a third channel is

available; it is useful to record the AMLR with one midline noninverting electrode (Fz) as well. Analysis then involves comparing the amplitude of Pa among these electrodes, especially between the hemispheres.

The amplitude of the Pa wave is mostly calculated using the peak-to-trough method rather than measuring the absolute

amplitude of Pa, because deﬁning a baseline for AMLR is dicult.3

The Na-Pa is the most widely used parameter in clinical analysis of AMLR. The interpeak latency (IPL) of the P0-Pa or Na-Pa may be a relevant parameter in assessing the integrity of the auditory pathway between midbrain and the auditory cortex. More recently, Weihing and coworkers,8 in their study on the relevant parameters for AMLR analysis in a large population of adults and

children, suggested ear and electrode eects as two additional

parameters that can be of clinical use in interpretation of AMLR, especially in children suspected of central auditory processing disorder (CAPD).

14.4.3 Nonpathologic Factors

Nonpathologic factors include test parameters and subject factors. Age in children younger than 10 years is the most important nonpathologic factor that must be considered in interpretation of the response normality. Maturation of the central auditory

nervous system has substantial eects on the detectability of the AMLR. In addition, the eects of age in neonates and young children interact with many other factors aecting the AMLR, particularly the stimulus rate and ﬁlter setting.

are required for recording AMLR from children under the age of

10, with rates as low as 0.5/s to 1/s for infants. ﬁlter setting, the spectral content of the EEG changes with age, and the low-frequency EEG activity may obscure the AMLR in

younger children. Therefore, using a higher frequency for high-

pass cuto decreases the variability of the response in children. For example, the detectability of AMLR is enhanced with 15-Hz compared to 3-Hz high-pass cuto. However, highly restricted ﬁltering—such as 30 to 100 Hz, which used to be applied in most early work with AMLR—may introduce an artiﬁcial component

to the response in the time range of the Pa component and must be avoided.

Sleep and sedation, the other important variables aecting the

AMLR in infants and young children, must be considered in interpretation of results.3 There is general agreement that sleep does not prevent the consistent detection of AMLR in adults, although the amplitude of Pa is largest during rapid-eye-movement (REM) sleep. However, in infants and young children, AMLR is variable and may not be detectable during sleep. In children, Pa can be detected during sleep stages 1 and 2, and REM sleep, but this

component is undetectable during phase 4 of sleep. The absence

of Pa is highly related to delta activity in the brain.9 The age at which Pa can be reliably recorded in children is highly variable;

in some children, a reliable Pa has been recorded in stage 4 sleep as young as 7 years old, while in some other children, no reliable Pa could be detected in stage 4 sleep until the age of 9 years. In

general, the detectability of AMLR in sleep increases from infancy to adolescence.

The distinct eects of sleep on the AMLR in adults versus children might originate from the contribution of dierent neural generators in the AMLR at dierent ages. It seems that AMLR in

younger children mostly arises from the activity of subcortical structures, particularly the reticular formation, and therefore is highly aected by sleep; however, as the thalamocortical generators mature, the AMLR is dominated by the activity of these structures, and the response becomes stable, even during sleep.

Developmental changes aecting AMLR are discussed later. In

general, clinical measurement of AMLR requires a constant state of arousal during the recording session. This can be a challenge in recording AMLR from infants and young children; age-appropriate animations are helpful to engage children’s attention and prevent them from falling asleep.

Regarding the

Pitfalls

Age and state of arousal, including sleep, are major factors in

•

AMLR measurement. Valid AMLR recordings are not possible in children who are

•

sedated or under general anesthesia.

Considering the dominant age eects, modiﬁcation of some

test parameters is a key factor in consistent detection of AMLR

in pediatric population. For example, stimulus rates of 8/s to 11/s

that are optimal for adults may be too fast for recording AMLR

in infants and young children. In general, rates of less than 5/s

14.4.4 Application in Pediatric

Populations

Another comment about terminology is warranted here.

The phrase “middle latency response,” abbreviated MLR, is

sometimes found in the literature and everyday clinical vocab-

ulary. However, “AMLR” is more accurate.3 The nonspeciﬁc term “middle latency response” and abbreviation “MLR” encompass

sensory evoked responses in other modalities, such as somatosensory, visual, and even vestibular responses, that occur within the same general time frame as the AMLR.

Major components of AMLR, including Na, Pa, Nb, and Pb (also

referred to as P50), occur within an interval from 10 to 50 ms

after acoustic stimulation.3 Soon after its discovery,4 AMLR was

148

14 Clinical Measurement and Application of Cortical Auditory Evoked Responses

introduced as a tool for estimation of hearing sensitivity in pediatric populations.10 Unfortunately, most initial AMLR recordings in children were made with test protocols developed earlier for adults. The use of suboptimal test parameters for AMLR in infants and young children led to two rather distinct problems. In some cases, no AMLR was recorded in children with normal auditory function, usually because of inappropriately fast stimulus rates. Paradoxically, in other cases evidence of an apparent AMLR was recorded from children with severe auditory dysfunction who, in fact, had no AMLR. This latter error was typically the outcome of

inappropriately restricted ﬁlter settings characterized by excessively high setting for the high-pass ﬁlter cuto.

Nowadays, generators of the AMLR are mostly deﬁned, and

developmental changes of the response associated with maturation of the CNS from infancy through adolescence are well documented. Therefore, consistent detection of response in young

children is guaranteed by modiﬁcation of some parameters in the

clinical protocol of AMLR measurement.

Pearl

Recent research conrms the sensitivity and specicity of the

AMLR in the electrophysiologic assessment of central auditory function in children suspected of auditory processing disorders (APD). Clinical practice guidelines support this application of AMLR.

Pa component generators are located bilaterally in the primary auditory cortices, that is, the Heschl gyri. This prominent AMLR component receives additional contributions from subcortical thalamic and reticular formation structures. According to Kraus and colleagues,

increases from 20% in infants to 90% in 12-year-old adolescents,

a trend that occurs whether the child develops normally or with cognitive, neurologic, or speech-language disorders. Latency of Pa

in infants is usually twice the adult values (about 50 ms), and the

waveform is morphologically broader than in adults, even under optimized measurement conditions. Throughout childhood, Pa amplitude increases and latency decreases until they reach adult values at about 10 years of age.

the likelihood of recording a Pa component

Nb and Pb Components

Sources of the Nb are still not clearly deﬁned, but they are

thought to be located in the secondary auditory cortex.3 The Pb component, which is probably the same wave as P1 of the ALR, derives from the auditory cortex, most likely the posterior region of the planum temporale within the temporal lobe. Pb has

a dierent course of development than Pa does. It is present as

early as 1 to 2 months of age, at very delayed latency values in comparison to adult expectations, and it continues to develop up to the age of 20 years.

14.4.5 Anatomic Generators and Developmental Changes

AMLRs arise from multiple generating systems, including both primary and secondary or nonprimary areas in the auditory thalamocortical pathways. AMLR waveforms arising from dif-

ferent generators have, not surprisingly, dierent time courses

of development. The nonprimary components develop earlier in life and depend on the sleep state, whereas the development of the primary components continues up to 10 to 12 years of age, and these components can be recorded during sleep.3 As a result, morphology, amplitude, and presence of AMLR waveforms dramatically change with age in children younger than 10 years. In fact, the probability of AMLR recording consistently increases with age from infancy to adulthood.

Na and Pa Components

Accumulated ﬁndings from research on AMLR generators suggest that Na originates from subcortical regions, including the thalamus, with great contribution from the inferior colliculus within the midbrain.8 The most prominent components of AMLR in children within the P0-Na complex are even detectible by the 33rd fetal week.3 Latency of the Na component decreases from

28 ms at about 30 weeks postconception to 20 ms at birth. The Na component ﬁnally decreases to 18 ms by the age of 3 months,

and then it remains stable into adulthood.

14.4.6 Clinical Applications of AMLR in Pediatric Population

In general, clinical applications of the AMLR can be divided into four categories: (1) assessment of hearing sensitivity, (2) neurodiagnosis, (3) documentation of cochlear implant (CI) and

validation of auditory training eects, and (4) monitoring depth of anesthesia. Each of these applications is now reviewed briey.

Estimation of Hearing Threshold

Historically, during the late 1960s and early 1970s, estimation of

hearing threshold was the most widespread clinical application of AMLR. instrumentation, interest in the clinical application of AMLR for threshold estimation waned as the ABR took over the stage. The main reason for this rapid transition to the use of ABR was the then unique possibility of recording the response during sleep or under sedation. This was a very attractive advantage for audiologists at the time, because recording a reliable AMLR from an

awake child was very challenging given the eects of myogenic

and movement artifacts on the response. Unfortunately, AMLR

is also highly susceptible to the eects of sleep, especially in

infants and young children.

cation of AMLR in estimating low-frequency hearing thresholds

because clinical experience conﬁrmed that the ABR was highly

dependent on neural synchrony.3 As a result, low-frequency tone

bursts with their low onsets were not very eective in eliciting a robust ABR. AMLR oered several advantages as a tool for

3,10

However, with the advent of ABR and its clinical

Later, there was a modest amount of renewed interest in appli-

149

II Diagnosing Hearing Disorders in Infants and Children

assessment of hearing thresholds at low frequencies. First, the amplitude of the AMLR Pa was twice that of the ABR wave V, so the response could be reliably detected at lower levels with less averaging. Second, AMLR could be elicited by longer-duration tone

bursts with higher frequency speciﬁcity, as it is not as dependent

on neural synchrony as the ABR is.

Finally, the AMLR could be recorded using the same instrumentation as ABR. Emergence in the late 1980s of clinical instrumentation for recording the auditory steady-state response (ASSR) contributed further to a reduction in this application of AMLR in pediatric population. According to the guidelines of the Joint Committee on Infant Hearing,12 tone burst–evoked ABR and ASSR evoked with amplitude- and frequency-modulated (FM) pure tone

signals are now the techniques of choice for frequency-speciﬁc

hearing threshold estimation.

Cochlear Implantation

Kileny et al in 1989 ﬁrst suggested the AMLR as a tool for assessment of CI ecacy.13 These researchers showed that the wave-

form for an electrically elicited AMLR, abbreviated as EAMLR, has comparable morphology and latencies as the acoustically

evoked AMLR. The EAMLR oers three strengths as an objective

method for evaluation of auditory function in CI users. The longer latencies of AMLR components Na and Pa separate them from electrical stimulus artifact, which is a major problem with ABR. Second, the possibility of using longer pulse trains with AMLR

results in lower thresholds. Last, since “we hear with our brains”

and the AMLR is generated in a very important region of the auditory cortex in addition to the upper brainstem, it provides a

more complete assessment of the subject’s “hearing” ability than

the ABR.

the assessment of changes in auditory function of children as a result of cochlear implantation. The authors evaluated 50 children with CIs with the AMLR at the time of surgery and several times during one year after receiving implantation. Another

subject group consisted of 31 other children who had 5 years of

implant experience, with AMLRs that were barely detected at the time of surgery under anesthesia. Within this group, AMLRs were

detected in only 35% of users right after the activation of their

device, whereas after at least one year of implant use detectabil-

ity of AMLR reached 100%. The ﬁnding of AMLR improvement

after a period of CI activation suggests activity-dependent plasticity of the auditory thalamocortical pathways as a result of receiving auditory stimulation. In addition, there is evidence that postlingually deafened implant users have AMLRs with larger amplitudes and shorter latencies compared to prelingually deafened users.

cochlear implantation, since it is considered to be the physiologic marker of the auditory thalamocortical development. In general,

children with longer times of using CIs have lower P50 latencies,16 and the development pattern of the P50 in children after activation

of their implant also follows the same developmental pattern as normal-hearing children with some delay in maturation. Research

ﬁndings conﬁrm that children who are implanted during the sensitive period show a very rapid development of P50, with latency reaching normal values within only 6 to 8 months following the

Gordon and colleagues14 conducted the ﬁrst study of AMLR in

The Pb (P50) wave has been applied in evaluating the eect of

implantation, a more rapid rate of development than observed

in normal-hearing children.

This ﬁnding might reect synaptic

plasticity, widespread activation of all layers of the auditory cortex, and improvement in neural synchronization as a result of receiving the electrical stimulation during the sensitive period.

Neurodiagnosis

AMLR has been used as a tool for assessing the integrity of the auditory pathway from the thalamus to the auditory cortex. Neurodiagnostic application of AMLR is based on the analysis of latency and, especially, amplitude, mostly of the AMLR Pa component recorded from the midline and hemisphere electrodes. As reviewed earlier in this chapter, amplitude is more reliable and is the parameter of choice for neurodiagnostic applications of AMLR. The amplitude of the Pa component in normal individuals is symmetric over the hemispheres. In neurodiagnostic application of AMLR the amplitude of Pa is compared among the noninverting electrodes over the hemispheres, such as C3 and

C4 and midline electrodes such as Fz or Cz. Amplitude of Pa is considered to be abnormal if it is reduced to 50% in one of these

locations in comparison to a waveform recorded in another electrode location. The other criterion for abnormality is a Pa component with the amplitude value of less than that of wave V of ABR with stimulation of the same ear. An abnormally reduced Pa on left or right hemisphere is consisted with a dysfunction in the thalamocortical pathway on that side, whether stimulation is presented to the right ear or to the left ear.

3,8

Selected studies

on this neurodiagnostic application of AMLR are now reviewed.

Auditory Processing, Learning, and Language Disorders

Since the AMLR is the earliest auditory cortical response, it has attracted considerable attention and is considered the most important auditory evoked response for diagnosing and understanding the CAPD. A handful of studies have investigated the AMLR in assessing children with learning disabilities and speech and/or language disorders. Research evidence has led to recommendations for incorporating AMLR into the test battery for assessment of CAPD.

Schochat and colleagues19 compared AMLR ﬁndings for a group

of 30 children aged from 8 to 14 years old who were diagnosed

with CAPD based on their performance on behavioral central auditory tests versus 22 normal-hearing children without CAPD. The Na-Pa amplitude was signiﬁcantly smaller over the left hemisphere (i.e., C3) in the CAPD group compared to the control group. The children diagnosed with CAPD were then enrolled in an auditory training program for 2 months that included frequency, intensity, temporal and speech perception training as well as a

dichotic task for interaural intensity dierence training. Ecacy

of the auditory training was evaluated using behavioral tests and AMLR. The results showed improved performance of the CAPD

group on behavioral tests conﬁrmed by the AMLR. Speciﬁcally,

Na-Pa amplitude increased on the left hemisphere of the CAPD

children, with the result that there was no dierence between

groups after training.

Purdy and coworkers20 evaluated central auditory processing in

a group of children diagnosed with learning disability (LD) using

150

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