Test–Retest Reliability of Dual-Recorded Brainstem versus Cortical Auditory-Evoked Potentials to Speech

Abstract

Background:

Auditory-evoked potentials have proven useful in the objective evaluation of sound encoding at different stages of the auditory pathway (brainstem and cortex). Yet, their utility for use in clinical assessment and empirical research relies critically on the precision and test–retest repeatability of the measure.

Purpose:

To determine how subcortical/cortical classes of auditory neural responses directly compare in terms of their internal consistency and test–retest reliability within and between listeners.

Research Design:

A descriptive cohort study describing the dispersion of electrophysiological measures.

Study Sample:

Eight young, normal-hearing female listeners.

Data Collection and Analysis:

We recorded auditory brainstem responses (ABRs), brainstem frequency-following responses (FFRs), and cortical (P1-N1-P2) auditory-evoked potentials elicited by speech sounds in the same set of listeners. We reassessed responses within each of four different test sessions over a period of 1 mo, allowing us to detect possible changes in latency/amplitude characteristics with finer detail than in previous studies.

Results:

Our findings show that brainstem and cortical amplitude/latency measures are remarkably stable; with the exception of slight prolongation of the P1 wave, we found no significant variation in any response measure. Intraclass correlation analysis revealed that the speech-evoked FFR amplitude and latency measures achieved superior repeatability (intraclass correlation coefficient >0.85) among the more widely used obligatory brainstem (ABR) and cortical (P1-N1-P2) auditory-evoked potentials. Contrasting these intersubject effects, intrasubject variability (i.e., within-subject coefficient of variation) revealed that while latencies were more stable than amplitudes, brainstem and cortical responses did not differ in their variability at the single subject level.

Conclusions:

We conclude that (1) the variability of auditory neural responses increases with ascending level along the auditory neuroaxis (cortex > brainstem) between subjects but remains highly stable within subjects and (2) speech-FFRs might provide a more stable measure of auditory function than other conventional responses (e.g., click-ABR), given their lower inter- and intrasubject variability.

Key Words

auditory brainstem response - event-related brain potentials - frequency-following response - intraclass correlation coefficient - test–retest reliability

This work was supported by grants from the American Hearing Research Foundation (AHRF) and American Academy of Audiology (AAA) Foundation awarded to G.M.B.

• REFERENCES

• Akhoun I, Gallégo S, Moulin A, Ménard M, Veuillet E, Berger-Vachon C, Collet L, Thai-Van H. 2008; The temporal relationship between speech auditory brainstem responses and the acoustic pattern of the phoneme /ba/ in normal-hearing adults. Clin Neurophysiol 119 (04) 922-933
• Alain C, Roye A, Arnott SR. 2013. Middle- and long-latency auditory evoked potentials: What are they telling us on central auditory disorders?. In: Celesia GG. Handbook of Clinical Neurophysiology: Disorders of Peripheral and Central Auditory Processing. The Netherlands: Elsevier
• Banai K, Abrams D, Kraus N. 2007; Sensory-based learning disability: insights from brainstem processing of speech sounds. Int J Audiol 46 (09) 524-532
• Banai K, Hornickel J, Skoe E, Nicol T, Zecker S, Kraus N. 2009; Reading and subcortical auditory function. Cereb Cortex 19 (11) 2699-2707
• Basu M, Krishnan A, Weber-Fox C. 2010; Brainstem correlates of temporal auditory processing in children with specific language impairment. Dev Sci 13 (01) 77-91
• Bidelman GM. 2014; Objective information-theoretic algorithm for detecting brainstem-evoked responses to complex stimuli. J Am Acad Audiol 25 (08) 715-726
• Bidelman GM, Moreno S, Alain C. 2013; Tracing the emergence of categorical speech perception in the human auditory system. Neuroimage 79: 201-212
• Bidelman GM. 2015; a Towards an optimal paradigm for simultaneously recording cortical and brainstem auditory evoked potentials. J Neurosci Methods 241: 94-100
• Bidelman GM. 2015; b Multichannel recordings of the human brainstem frequency-following response: scalp topography, source generators, and distinctions from the transient ABR. Hear Res 323: 68-80
• Bidelman GM. 2017. Communicating in challenging environments: noise and reverberation. In: Kraus N, Anderson S, White-Schwoch T, Fay RR, Popper AN. Springer Handbook of Auditory Research: The Frequency-Following Response: A Window into Human Communication. New York, NY: Springer Nature.
• Bidelman GM, Alain C. 2015; Musical training orchestrates coordinated neuroplasticity in auditory brainstem and cortex to counteract age-related declines in categorical vowel perception. J Neurosci 35 (03) 1240-1249
• Bidelman GM, Villafuerte JW, Moreno S, Alain C. 2014; Age-related changes in the subcortical-cortical encoding and categorical perception of speech. Neurobiol Aging 35 (11) 2526-2540
• Bidelman GM, Weiss MW, Moreno S, Alain C. 2014; Coordinated plasticity in brainstem and auditory cortex contributes to enhanced categorical speech perception in musicians. Eur J Neurosci 40 (04) 2662-2673
• Bornstein MH, Rothstein H, Cohen J. 1997 Power and Precision™ (v1) [Computer software], Biostat, Englewood, NJ
• Caruso S, Maiolino L, Rugolo S, Intelisano G, Farina M, Cocuzza S, Serra A. 2003; Auditory brainstem response in premenopausal women taking oral contraceptives. Hum Reprod 18 (01) 85-89
• Cassidy SM, Robertson IH, O’Connell RG. 2012; Retest reliability of event-related potentials: evidence from a variety of paradigms. Psychophysiology 49 (05) 659-664
• Chandrasekaran B, Kraus N. 2010; The scalp-recorded brainstem response to speech: neural origins and plasticity. Psychophysiology 47 (02) 236-246
• Cicchetti DV. 1994; Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. Psychol Assess 6: 284-290
• Cunningham J, Nicol T, King C, Zecker SG, Kraus N. 2002; Effects of noise and cue enhancement on neural responses to speech in auditory midbrain, thalamus and cortex. Hear Res 169 1–2 97-111
• Dalebout SD, Robey RR. 1997; Comparison of the intersubject and intrasubject variability of exogenous and endogenous auditory evoked potentials. J Am Acad Audiol 8 (05) 342-354
• Edwards RM, Buchwald JS, Tanguay PE, Schwafel JA. 1982; Sources of variability in auditory brain stem evoked potential measures over time. Electroencephalogr Clin Neurophysiol 53 (02) 125-132
• Elkind-Hirsch KE, Stoner WR, Stach BA, Jerger JF. 1992; Estrogen influences auditory brainstem responses during the normal menstrual cycle. Hear Res 60 (02) 143-148
• Galbraith GC, Arbagey PW, Branski R, Comerci N, Rector PM. 1995; Intelligible speech encoded in the human brain stem frequency-following response. Neuroreport 6 (17) 2363-2367
• Galbraith GC, Brown WS. 1990; Cross-correlation and latency compensation analysis of click-evoked and frequency-following brain-stem responses in man. Electroencephalogr Clin Neurophysiol 77 (04) 295-308
• Hall JW. 1992. Handbook of Auditory Evoked Responses. Needham Heights, MA: Allyn and Bacon;
• Hall MH, Schulze K, Rijsdijk F, Picchioni M, Ettinger U, Bramon E, Freedman R, Murray RM, Sham P. 2006; Heritability and reliability of P300, P50 and duration mismatch negativity. Behav Genet 36 (06) 845-857
• Hillyard SA, Picton TW. 1979. Event-related brain potentials and selective information processing in man. In: Desmedt JE. Progress in Clinical Neurophysiology. Basel, Switzerland: Karger;
• Hoormann J, Falkenstein M, Hohnsbein J, Blanke L. 1992; The human frequency-following response (FFR): normal variability and relation to the click-evoked brainstem response. Hear Res 59 (02) 179-188
• Hornickel J, Knowles E, Kraus N. 2012; Test-retest consistency of speech-evoked auditory brainstem responses in typically-developing children. Hear Res 284 1–2 52-58
• Hu L, Mouraux A, Hu Y, Iannetti GD. 2010; A novel approach for enhancing the signal-to-noise ratio and detecting automatically event-related potentials (ERPs) in single trials. Neuroimage 50 (01) 99-111
• Huffmeijer R, Bakermans-Kranenburg MJ, Alink LRA, van Ijzendoorn MH. 2014; Reliability of event-related potentials: the influence of number of trials and electrodes. Physiol Behav 130: 13-22
• Jerger J, Jerger S. 1985; Audiologic applications of early, middle, and late auditory evoked potentials. Hear J 38: 31-36
• Jerger J, Musiek F. 2000; Report of the consensus conference on the diagnosis of auditory processing disorders in school-aged children. J Am Acad Audiol 11 (09) 467-474
• Klatt DH, Klatt LC. 1990; Analysis, synthesis, and perception of voice quality variations among female and male talkers. J Acoust Soc Am 87 (02) 820-857
• Koch GG. 1982. Intraclass correlation coefficient. In: Kotz S, Johnson NL. Encyclopedia of Statistical Sciences. New York, NY: John Wiley & Sons;
• Kraus N, Anderson S, White-Schwoch T, Fay RR, Popper AN. 2017. The Frequency-Following Response: A Window into Human Communication. New York, NY: Springer Nature.
• Krishnan A. 2007. Human frequency following response. In: Burkard RF, Don M, Eggermont JJ. Auditory Evoked Potentials: Basic Principles and Clinical Application. Baltimore, MD: Lippincott Williams & Wilkins;
• Krizman JL, Skoe E, Kraus N. 2010; Stimulus rate and subcortical auditory processing of speech. Audiol Neurootol 15 (05) 332-342
• Lauter JL, Karzon RG. 1990; a Individual differences in auditory electric responses: comparisons of between-subject and within-subject variability. V. Amplitude-variability comparisons in early, middle, and late responses. Scand Audiol 19 (04) 201-206
• Lauter JL, Karzon RG. 1990; b Individual differences in auditory electric responses: comparisons of between-subject and within-subject variability. IV. Latency-variability comparisons in early, middle, and late responses. Scand Audiol 19 (03) 175-182
• Lightfoot G, Kennedy V. 2006; Cortical electric response audiometry hearing threshold estimation: accuracy, speed, and the effects of stimulus presentation features. Ear Hear 27 (05) 443-456
• McEvoy LK, Smith ME, Gevins A. 2000; Test-retest reliability of cognitive EEG. Clin Neurophysiol 111 (03) 457-463
• McEwen BS, Davis PG, Parsons B, Pfaff DW. 1979; The brain as a target for steroid hormone action. Annu Rev Neurosci 2: 65-112
• McFadden KL, Steinmetz SE, Carroll AM, Simon ST, Wallace A, Rojas DC. 2014; Test-retest reliability of the 40 Hz EEG auditory steady-state response. PLoS One 9 (01) e85748
• McFarland DJ, Cacace AT. 2012; Questionable reliability of the speech-evoked auditory brainstem response (sABR) in typically-developing children. Hear Res 287 1–2 1-2, author reply 3–5
• McGraw KO, Wong SP. 1996; Forming inferences about some intraclass correlation coefficients. Psychol Methods 1: 30-46
• Musacchia G, Strait D, Kraus N. 2008; Relationships between behavior, brainstem and cortical encoding of seen and heard speech in musicians and non-musicians. Hear Res 241 1–2 34-42
• Näätänen R. 1992. Attention and Brain Function. Hillsdale, NJ: Lawrence Erlbaum Associates;
• Okamoto H, Stracke H, Bermudez P, Pantev C. 2011; Sound processing hierarchy within human auditory cortex. J Cogn Neurosci 23 (08) 1855-1863
• Oyler RF, Lauter JL, Matkin ND. 1991; Intrasubject variability in the absolute latency of the auditory brainstem response. J Am Acad Audiol 2 (04) 206-213
• Picton TW. 2010. Human Auditory Evoked Potentials. 1st ed. San Diego, CA: Plural Publishing;
• Picton TW, Alain C, Woods DL, John MS, Scherg M, Valdes-Sosa P, Bosch-Bayard J, Trujillo NJ. 1999; Intracerebral sources of human auditory-evoked potentials. Audiol Neurootol 4 (02) 64-79
• Picton TW, Hillyard SA. 1974; Human auditory evoked potentials. II. Effects of attention. Electroencephalogr Clin Neurophysiol 36 (02) 191-200
• Picton TW, Hillyard SA, Galambos R, Schiff M. 1971; Human auditory attention: a central or peripheral process?. Science 173 3994 351-353
• Picton TW, Woods DL, Baribeau-Braun J, Healey TM. 1976; Evoked potential audiometry. J Otolaryngol 6 (02) 90-119
• Picton TW, Woods DL, Proulx GB. 1978; Human auditory sustained potentials. II. Stimulus relationships. Electroencephalogr Clin Neurophysiol 45 (02) 198-210
• Ponton CW, Eggermont JJ, Kwong B, Don M. 2000; Maturation of human central auditory system activity: evidence from multi-channel evoked potentials. Clin Neurophysiol 111 (02) 220-236
• Rocha-Muniz CN, Befi-Lopes DM, Schochat E. 2012; Investigation of auditory processing disorder and language impairment using the speech-evoked auditory brainstem response. Hear Res 294 1–2 143-152
• Rocha-Muniz CN, Befi-Lopes DM, Schochat E. 2014; Sensitivity, specificity and efficiency of speech-evoked ABR. Hear Res 317: 15-22
• Russo N, Nicol T, Musacchia G, Kraus N. 2004; Brainstem responses to speech syllables. Clin Neurophysiol 115 (09) 2021-2030
• Salinsky MC, Oken BS, Morehead L. 1991; Test-retest reliability in EEG frequency analysis. Electroencephalogr Clin Neurophysiol 79 (05) 382-392
• Scherg M, Vajsar J, Picton TW. 1989; A source analysis of the late human auditory evoked potentials. J Cogn Neurosci 1 (04) 336-355
• Sininger YS, Abdala C, Cone-Wesson B. 1997; Auditory threshold sensitivity of the human neonate as measured by the auditory brainstem response. Hear Res 104 1–2 27-38
• Skoe E, Kraus N. 2010; Auditory brain stem response to complex sounds: a tutorial. Ear Hear 31 (03) 302-324
• Song JH, Banai K, Russo NM, Kraus N. 2006; On the relationship between speech- and nonspeech-evoked auditory brainstem responses. Audiol Neurootol 11 (04) 233-241
• Song JH, Nicol T, Kraus N. 2011; Test-retest reliability of the speech-evoked auditory brainstem response. Clin Neurophysiol 122 (02) 346-355
• Stapells DR. 2000; Threshold estimation by the tone-evoked auditory brainstem response: a literature meta-analysis. J Speech Lang Pathol Audiol 42: 74-83
• Starr A, Picton TW, Sininger Y, Hood LJ, Berlin CI. 1996; Auditory neuropathy. Brain 119 Pt 3 741-753
• Tervaniemi M, Sinkkonen J, Virtanen J, Kallio J, Ilmoniemi RJ, Salonen O, Näätänen R. 2005; Test-retest stability of the magnetic mismatch response (MMNm). Clin Neurophysiol 116 (08) 1897-1905
• Thornton ARD, Coleman MJ. 1975; The adaptation of cochlear and brainstem auditory evoked potentials in humans. Electroencephalogr Clin Neurophysiol 39 (04) 399-406
• Tremblay KL, Friesen L, Martin BA, Wright R. 2003; Test-retest reliability of cortical evoked potentials using naturally produced speech sounds. Ear Hear 24 (03) 225-232
• Walhovd KB, Fjell AM. 2002; One-year test-retest reliability of auditory ERPs in young and old adults. Int J Psychophysiol 46 (01) 29-40
• Weiss MW, Bidelman GM. 2015; Listening to the brainstem: musicianship enhances intelligibility of subcortical representations for speech. J Neurosci 35 (04) 1687-1691
• Williams LM, Simms E, Clark CR, Paul RH, Rowe D, Gordon E. 2005; The test-retest reliability of a standardized neurocognitive and neurophysiological test battery: “neuromarker.”. Int J Neurosci 115 (12) 1605-1630
• Woods DL, Hillyard SA. 1978. Attention at the cocktail party: brainstem evoked responses reveal no peripheral gating. In: Otto DA. Multidisciplinary Perspectives in Event-Related Brain Potential Research (EPA 600/9-77-043). Washington, DC: U.S. Government Printing Office;
• Yadav A, Tandon OP, Vaney N. 2003; Long latency auditory evoked responses in ovulatory and anovulatory menstrual cycle. Indian J Physiol Pharmacol 47 (02) 179-184