Analyzing the FFR: A tutorial for decoding the richness of auditory function

The frequency-following response, or FFR, is a neurophysiological response to sound that precisely reflects the ongoing dynamics of sound. It can be used to study the integrity and malleability of neural encoding of sound across the lifespan. Sound processing in the brain can be impaired with pathology and enhanced through expertise. The FFR can index linguistic deprivation, autism, concussion, and reading impairment, and can reflect the impact of enrichment with short-term training, bilingualism, and musicianship. Because of this vast potential, interest in the FFR has grown considerably in the decade since our first tutorial. Despite its widespread adoption, there remains a gap in the current knowledge of its analytical potential. This tutorial aims to bridge this gap. Using recording methods we have employed for the last 20 + years, we have explored many analysis strategies. In this tutorial, we review what we have learned and what we think constitutes the most effective ways of capturing what the FFR can tell us. The tutorial covers FFR components (timing, fundamental frequency, harmonics) and factors that influence FFR (stimulus polarity, response averaging, and stimulus presentation/recording jitter). The spotlight is on FFR analyses, including ways to analyze FFR timing (peaks, autocorrelation, phase consistency, cross-phaseogram), magnitude (RMS, SNR, FFT), and fidelity (stimulus-response correlations, response-to-response correlations and response consistency). The wealth of information contained within an FFR recording brings us closer to understanding how the brain reconstructs our sonic world.

[1]  Jennifer Krizman,et al.  Auditory biological marker of concussion in children , 2016, Scientific Reports.

[2]  G C Galbraith,et al.  Speech-evoked brainstem frequency-following responses during verbal transformations due to word repetition. , 1997, Electroencephalography and clinical neurophysiology.

[3]  Yisheng Xu,et al.  Human frequency-following response: representation of pitch contours in Chinese tones , 2004, Hearing Research.

[4]  N. Kraus,et al.  The Frequency-Following Response: A Window into Human Communication , 2017 .

[5]  Jennifer Krizman,et al.  Music training alters the course of adolescent auditory development , 2015, Proceedings of the National Academy of Sciences.

[6]  Erika Skoe,et al.  Neural Processing of Speech Sounds in ASD and First-Degree Relatives , 2010, Journal of Autism and Developmental Disorders.

[7]  Richard F. Lyon,et al.  A computational model of filtering, detection, and compression in the cochlea , 1982, ICASSP.

[8]  Alan R Palmer,et al.  Phase-locked responses to pure tones in the inferior colliculus. , 2006, Journal of neurophysiology.

[9]  N. Kraus,et al.  Music training for the development of auditory skills , 2010, Nature Reviews Neuroscience.

[10]  A. Krishnan,et al.  The role of the auditory brainstem in processing linguistically-relevant pitch patterns , 2009, Brain and Language.

[11]  Nicole M. Russo,et al.  Musical experience shapes human brainstem encoding of linguistic pitch patterns , 2007, Nature Neuroscience.

[12]  Frequency-following response among neonates with progressive moderate hyperbilirubinemia , 2019, Journal of Perinatology.

[13]  N. Kraus,et al.  Children with autism spectrum disorder have unstable neural responses to sound , 2018, Experimental Brain Research.

[14]  N. Kraus,et al.  Neurobiology of Everyday Communication: What Have We Learned From Music? , 2017, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[15]  N. Kraus,et al.  Case studies in neuroscience: Subcortical origins of the frequency-following response. , 2019, Journal of neurophysiology.

[16]  D. Abrams,et al.  Individual Differences in Human Auditory Processing: Insights From Single‐Trial Auditory Midbrain Activity in an Animal Model , 2017, Cerebral cortex.

[17]  G. Prendergast,et al.  Speech Auditory Brainstem Responses: Effects of Background, Stimulus Duration, Consonant–Vowel, and Number of Epochs , 2019, Ear and hearing.

[18]  Gavin M. Bidelman,et al.  Subcortical sources dominate the neuroelectric auditory frequency-following response to speech , 2018, NeuroImage.

[19]  N. Kraus,et al.  Reversal of age-related neural timing delays with training , 2013, Proceedings of the National Academy of Sciences.

[20]  Mikolaj Kegler,et al.  Decoding of selective attention to continuous speech from the human auditory brainstem response , 2019, NeuroImage.

[21]  Erika Skoe,et al.  Plasticity in the Adult Human Auditory Brainstem following Short-term Linguistic Training , 2008, Journal of Cognitive Neuroscience.

[22]  N. Kraus,et al.  Reading and subcortical auditory function. , 2009, Cerebral cortex.

[23]  David Poeppel,et al.  The coupling between auditory and motor cortices is rate-restricted: Evidence for an intrinsic speech-motor rhythm , 2018, Science Advances.

[24]  P. Cariani,et al.  Encoding of pitch in the human brainstem is sensitive to language experience. , 2005, Brain research. Cognitive brain research.

[25]  Erika Skoe,et al.  Stability and plasticity of auditory brainstem function across the lifespan. , 2015, Cerebral cortex.

[26]  N. Kraus,et al.  The scalp-recorded brainstem response to speech: neural origins and plasticity. , 2010, Psychophysiology.

[27]  Erika Skoe,et al.  Brainstem encoding of voiced consonant–vowel stop syllables , 2008, Clinical Neurophysiology.

[28]  Adam Tierney,et al.  Successful non-native speech perception is linked to frequency following response phase consistency , 2017, Cortex.

[29]  T. Picton,et al.  Human auditory steady-state responses to amplitude-modulated tones: phase and latency measurements , 2000, Hearing Research.

[30]  N. Kraus,et al.  Subcortical encoding of sound is enhanced in bilinguals and relates to executive function advantages , 2012, Proceedings of the National Academy of Sciences.

[31]  R. P. Carlyon,et al.  Subcortical Neural Synchrony and Absolute Thresholds Predict Frequency Discrimination Independently , 2013, Journal of the Association for Research in Otolaryngology.

[32]  S. Gordon-Salant,et al.  Age Effects on Neural Representation and Perception of Silence Duration Cues in Speech. , 2019, Journal of speech, language, and hearing research : JSLHR.

[33]  N. Kraus,et al.  Musical Training Enhances Neural Processing of Binaural Sounds , 2013, The Journal of Neuroscience.

[34]  R. Kulesza,et al.  Characterization of the human central nucleus of the inferior colliculus , 2019, Hearing Research.

[35]  N. Kraus,et al.  Hearing It Again and Again: On-Line Subcortical Plasticity in Humans , 2010, PloS one.

[36]  N. Kraus,et al.  Brainstem correlates of speech-in-noise perception in children , 2010, Hearing Research.

[37]  Nina Kraus,et al.  The Ability to Move to a Beat Is Linked to the Consistency of Neural Responses to Sound , 2013, The Journal of Neuroscience.

[38]  N. Kraus,et al.  Musical experience and neural efficiency – effects of training on subcortical processing of vocal expressions of emotion , 2009, The European journal of neuroscience.

[39]  J J Eggermont,et al.  Measuring human cochlear traveling wave delay using distortion product emission phase responses. , 1993, The Journal of the Acoustical Society of America.

[40]  Tobias Reichenbach,et al.  The human auditory brainstem response to running speech reveals a subcortical mechanism for selective attention , 2017, bioRxiv.

[41]  N. Kraus,et al.  The neural legacy of a single concussion , 2017, Neuroscience Letters.

[42]  G. Bidelman Multichannel recordings of the human brainstem frequency-following response: Scalp topography, source generators, and distinctions from the transient ABR , 2015, Hearing Research.

[43]  Jordi Costa-Faidella,et al.  The frequency-following response (FFR) to speech stimuli: A normative dataset in healthy newborns , 2019, Hearing Research.

[44]  G C Galbraith,et al.  Brain stem frequency‐following response to dichotic vowels during attention , 1998, Neuroreport.

[45]  N. Kraus,et al.  The Impoverished Brain: Disparities in Maternal Education Affect the Neural Response to Sound , 2013, The Journal of Neuroscience.

[46]  Hari M. Bharadwaj,et al.  A comparison of spectral magnitude and phase-locking value analyses of the frequency-following response to complex tones. , 2013, The Journal of the Acoustical Society of America.

[47]  M. Ruggero,et al.  Timing of spike initiation in cochlear afferents: dependence on site of innervation. , 1987, Journal of neurophysiology.

[48]  N. Kraus,et al.  Bilingual enhancements have no socioeconomic boundaries. , 2016, Developmental science.

[49]  C. Escera,et al.  Involvement of the Serotonin Transporter Gene in Accurate Subcortical Speech Encoding , 2016, The Journal of Neuroscience.

[50]  A. Tierney,et al.  Successful second language learning is tied to robust domain-general auditory processing and stable neural representation of sound , 2019, Brain and Language.

[51]  A. Friederici,et al.  Dyslexia risk gene relates to representation of sound in the auditory brainstem , 2017, Developmental Cognitive Neuroscience.

[52]  Sylvain Baillet,et al.  Cortical contributions to the auditory frequency-following response revealed by MEG , 2016, Nature Communications.

[53]  G C Galbraith,et al.  Intelligible speech encoded in the human brain stem frequency-following response. , 1995, Neuroreport.

[54]  Nicole M. Russo,et al.  Deficient brainstem encoding of pitch in children with Autism Spectrum Disorders , 2008, Clinical Neurophysiology.

[55]  N. Kraus,et al.  Musicians' enhanced neural differentiation of speech sounds arises early in life: developmental evidence from ages 3 to 30. , 2014, Cerebral cortex.

[56]  B. Rieger,et al.  Brainstem Evoked Potential Indices of Subcortical Auditory Processing After Mild Traumatic Brain Injury , 2017, Ear and hearing.

[57]  Nina Kraus,et al.  Brainstem responses to speech syllables , 2004, Clinical Neurophysiology.

[58]  Steven Greenberg,et al.  A space-time theory of pitch and timbre based on cortical expansion of the cochlear traveling wave delay , 1998 .

[59]  W Jesteadt,et al.  Auditory brainstem responses to tone bursts in normally hearing subjects. , 1988, Journal of speech and hearing research.

[60]  Terence W. Picton,et al.  Envelope and spectral frequency-following responses to vowel sounds , 2008, Hearing Research.

[61]  Jayashree S. Bhat,et al.  Effect of Stimulus Polarity on Speech Evoked Auditory Brainstem Response , 2013, Audiology research.

[62]  E. Skoe,et al.  Basic neural processing of sound in adults is influenced by bilingual experience , 2017, Neuroscience.

[63]  Erika Skoe,et al.  Frequency-dependent fine structure in the frequency-following response: The byproduct of multiple generators , 2017, Hearing Research.

[64]  N. Kraus,et al.  Clapping in time parallels literacy and calls upon overlapping neural mechanisms in early readers , 2018, Annals of the New York Academy of Sciences.

[65]  Jiong Hu,et al.  Cross-Linguistic Comparison of Frequency-Following Responses to Voice Pitch in American and Chinese Neonates and Adults , 2011, Ear and hearing.

[66]  N. Kraus,et al.  Auditory Processing in Noise: A Preschool Biomarker for Literacy , 2015, PLoS biology.

[67]  L. Collet,et al.  The temporal relationship between speech auditory brainstem responses and the acoustic pattern of the phoneme /ba/ in normal-hearing adults , 2008, Clinical Neurophysiology.

[68]  Christopher J. Plack,et al.  Subcortical Plasticity Following Perceptual Learning in a Pitch Discrimination Task , 2011, Journal of the Association for Research in Otolaryngology.

[69]  Nina Kraus,et al.  Test–retest reliability of the speech-evoked auditory brainstem response , 2011, Clinical Neurophysiology.

[70]  M. Malmierca,et al.  Neurons, Connections, and Microcircuits of the Inferior Colliculus , 2018 .

[71]  I. Peretz,et al.  Recording the human brainstem frequency-following-response in the free-field , 2017, Journal of Neuroscience Methods.

[72]  A. Tierney,et al.  High school music classes enhance the neural processing of speech , 2013, Front. Psychol..

[73]  Ananthanarayan Krishnan,et al.  Human frequency-following responses: representation of steady-state synthetic vowels , 2002, Hearing Research.

[74]  Nina Kraus,et al.  Deficits in auditory brainstem pathway encoding of speech sounds in children with learning problems , 2002, Neuroscience Letters.

[75]  N. Kraus,et al.  Sex differences in auditory subcortical function , 2012, Clinical Neurophysiology.

[76]  Shigeyuki Kuwada,et al.  Sources of the scalp-recorded amplitude-modulation following response. , 2002, Journal of the American Academy of Audiology.

[77]  N. Kraus,et al.  Musical Experience Limits the Degradative Effects of Background Noise on the Neural Processing of Sound , 2009, The Journal of Neuroscience.

[78]  C. Dong,et al.  Atypical longitudinal development of speech‐evoked auditory brainstem response in preschool children with autism spectrum disorders , 2019, Autism research : official journal of the International Society for Autism Research.

[79]  M. Sams,et al.  Musicians have enhanced subcortical auditory and audiovisual processing of speech and music , 2007, Proceedings of the National Academy of Sciences.

[80]  Patrick C. M. Wong,et al.  Learning Two Tone Languages Enhances the Brainstem Encoding of Lexical Tones , 2018, INTERSPEECH.

[81]  Lina R. Kubli,et al.  Performance on tests of central auditory processing by individuals exposed to high-intensity blasts. , 2012, Journal of rehabilitation research and development.

[82]  N. Kraus,et al.  Unraveling the Biology of Auditory Learning: A Cognitive–Sensorimotor–Reward Framework , 2015, Trends in Cognitive Sciences.

[83]  Nina Kraus,et al.  Effects of hearing loss on the subcortical representation of speech cues. , 2013, The Journal of the Acoustical Society of America.

[84]  N. Kraus,et al.  Stimulus Rate and Subcortical Auditory Processing of Speech , 2010, Audiology and Neurotology.

[85]  Hugo Merchant,et al.  Monkeys share the neurophysiological basis for encoding sound periodicities captured by the frequency-following response with humans , 2017, Scientific Reports.

[86]  Erika Skoe,et al.  Neural processing of speech in children is influenced by extent of bilingual experience , 2015, Neuroscience Letters.

[87]  Nina Kraus,et al.  Test-retest consistency of speech-evoked auditory brainstem responses in typically-developing children , 2012, Hearing Research.

[88]  N. Kraus,et al.  Bilingualism increases neural response consistency and attentional control: Evidence for sensory and cognitive coupling , 2014, Brain and Language.

[89]  N. Kraus,et al.  Sex differences in subcortical auditory processing emerge across development , 2019, Hearing Research.

[90]  N. Kraus,et al.  The auditory brainstem is a barometer of rapid auditory learning , 2013, Neuroscience.

[91]  P. Kuhl,et al.  Effects of formant proximity and stimulus prototypicality on the neural discrimination of vowels: Evidence from the auditory frequency-following response , 2019, Brain and Language.

[92]  Manuel S. Malmierca,et al.  Pattern-sensitive neurons reveal encoding of complex auditory regularities in the rat inferior colliculus , 2019, NeuroImage.

[93]  D. D. Greenwood Critical Bandwidth and the Frequency Coordinates of the Basilar Membrane , 1961 .

[94]  Erika Skoe,et al.  Neural Timing Is Linked to Speech Perception in Noise , 2010, The Journal of Neuroscience.

[95]  Nina Kraus,et al.  Inferior colliculus contributions to phase encoding of stop consonants in an animal model , 2011, Hearing Research.

[96]  M. Malmierca,et al.  Descending Connections of Auditory Cortex to the Midbrain and Brain Stem , 2011 .

[97]  P. Skarżyński,et al.  An Analysis of The Parameters Used In Speech ABR Assessment Protocols. , 2018, The journal of international advanced otology.

[98]  Erika Skoe,et al.  Cross-phaseogram: Objective neural index of speech sound differentiation , 2011, Journal of Neuroscience Methods.

[99]  H Pratt,et al.  Sources of frequency following responses (FFR) in man. , 1977, Electroencephalography and clinical neurophysiology.

[100]  A. Palmer,et al.  Phase-locking in the cochlear nerve of the guinea-pig and its relation to the receptor potential of inner hair-cells , 1986, Hearing Research.

[101]  Hari M. Bharadwaj,et al.  Report Why Middle-aged Listeners Have Trouble Hearing in Everyday Settings , 2022 .

[102]  N. Kraus,et al.  Unstable Representation of Sound: A Biological Marker of Dyslexia , 2013, The Journal of Neuroscience.