Abstract
Electrical stimulation of the auditory nerve with a cochlear implant (CI) is the method of choice for treatment of severe-to-profound hearing loss. Understanding how the human auditory cortex responds to CI stimulation is important for advances in stimulation paradigms and rehabilitation strategies. In this study, auditory cortical responses to CI stimulation were recorded intracranially in a neurosurgical patient to examine directly the functional organization of the auditory cortex and compare the findings with those obtained in normal-hearing subjects. The subject was a bilateral CI user with a 20-year history of deafness and refractory epilepsy. As part of the epilepsy treatment, a subdural grid electrode was implanted over the left temporal lobe. Pure tones, click trains, sinusoidal amplitude-modulated noise, and speech were presented via the auxiliary input of the right CI speech processor. Additional experiments were conducted with bilateral CI stimulation. Auditory event-related changes in cortical activity, characterized by the averaged evoked potential and event-related band power, were localized to posterolateral superior temporal gyrus. Responses were stable across recording sessions and were abolished under general anesthesia. Response latency decreased and magnitude increased with increasing stimulus level. More apical intracochlear stimulation yielded the largest responses. Cortical evoked potentials were phase-locked to the temporal modulations of periodic stimuli and speech utterances. Bilateral electrical stimulation resulted in minimal artifact contamination. This study demonstrates the feasibility of intracranial electrophysiological recordings of responses to CI stimulation in a human subject, shows that cortical response properties may be similar to those obtained in normal-hearing individuals, and provides a basis for future comparisons with extracranial recordings.
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References
Abrams DA, Nicol T, Zecker S, Kraus N (2008) Right-hemisphere auditory cortex is dominant for coding syllable patterns in speech. J Neurosci 28:3958–6395
Ahissar E, Ahissar M (2005) Processing of the temporal envelope of speech. In: König R, Heil P, Budinger E, Scheich H (eds) The auditory cortex: a synthesis of human and animal research. Erlbaum, Mahwah, pp 295–314
Ahissar E, Nagarajan S, Ahissar M, Protopapas A, Mahncke H, Merzenich MM (2001) Speech comprehension is correlated with temporal response patterns recorded from auditory cortex. Proc Natl Acad Sci U S A 98:13367–13372
Ashley HL (2000) Cochlear implants in the United Kingdom. Cochlear Implants Int 1:16–17
Avants B, Epstein CL, Gee JC (2006) Geodesic image normalization in the space of diffeomorphisms. In: Mathematical foundations of computational anatomy: geometrical and statistical methods for modelling biological shape variability, October 1 2006, Copenhagen, Denmark. MFCA’06 Workshop Proceedings 125–133
Avants B, Epstein CL, Grossman M, Gee JC (2008) Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Analysis 12:26–41
Beitel RE, Vollmer M, Raggio MW, Schreiner CE (2011) Behavioral training enhances cortical temporal processing in neonatally deafened juvenile cats. J Neurophysiol 106:944–959
Boothroyd A, Hanin L, Hnath T (1985) CUNY laser videodisk of everyday sentences. Speech and Hearing Sciences Research Center, City University of New York, New York
Brown CJ, Etler C, He S, O'Brien S, Erenberg S, Kim JR, Dhuldhoya AN, Abbas PJ (2008) The electrically evoked auditory change complex: preliminary results from nucleus cochlear implant users. Ear Hear 29:704–717
Brugge JF, Nourski KV, Oya H, Kawasaki H, Reale RA, Howard MA (2008a) Representation of sinusoidal amplitude modulated noise within the primary auditory (core) cortex of human. Society for Neuroscience 38th Annual Meeting. November 15–19, 2008, Washington, DC Program No. 566.6. 2008 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2008. Online
Brugge JF, Volkov IO, Oya H, Kawasaki H, Reale RA, Fenoy A, Steinschneider M, Howard MA III (2008b) Functional localization of auditory cortical fields of human: click-train stimulation. Hear Res 238:12–24
Brugge JF, Nourski KV, Oya H, Reale RA, Kawasaki H, Steinschneider M, Howard MA III (2009) Coding of repetitive transients by auditory cortex of Heschl’s gyrus of human. J Neurophysiol 102:2358–2374
Cervenka MC, Nagle S, Boatman-Reich D (2011) Cortical high-gamma responses in auditory processing. Am J Audiol 20:171–180
Crone NE, Boatman D, Gordon B, Hao L (2001) Induced electrocorticographic gamma activity during auditory perception. Clin Neurophysiol 112:565–582
Edwards E, Soltani M, Kim W, Dalal SS, Nagarajan SS, Berger MS, Knight RT (2009) Comparison of time-frequency responses and the event-related potential to auditory speech stimuli in human cortex. J Neurophysiol 102:377–386
Engel AK, Moll CK, Fried I, Ojemann GA (2005) Invasive recordings from the human brain: clinical insights and beyond. Nat Rev Neurosci 6:35–47
Fallon J, Irvine D, Coco A, Donley L, Millard R, Shepherd R (2007) Cochlear implantation influences the temporal responsiveness of the primary auditory cortex in the deafened cat. Assoc. Res. Otolaryngol. 2007 MidWinter Meeting. February 10–15, 2007, Denver, CO. Assoc. Res. Otolaryngol Abs: 507
Fallon JB, Irvine DR, Shepherd RK (2009) Neural prostheses and brain plasticity. J Neural Eng 6:065008
Fayad JN, Linthicum FH (2006) Multichannel cochlear implants: relation of histopathology to performance. Laryngoscope 116:1310–1320
Firszt JB, Chambers RD, Kraus N, Reeder RM (2002) Neurophysiology of cochlear implant users I: effects of stimulus current level and electrode site on the electrical ABR, MLR and N1-P2 response. Ear Hear 23:502–515
Fu QJ (2002) Temporal processing and speech recognition in cochlear implant users. Neuroreport 13:1635–1639
Gilley PM, Sharma A, Dorman M, Finley CC, Panch AS, Martin K (2006) Minimization of cochlear implant stimulus artifact in cortical auditory evoked potentials. Clin Neurophysiol 117:1949–56
Giraud AL, Truy E, Frackowiak R (2001) Imaging plasticity in cochlear implant patients. Audiol Neurootol 6:381–393
Greenlee JD, Jackson AW, Chen F, Larson CR, Oya H, Kawasaki H, Chen H, Howard MA III (2011) Human auditory cortical activation during self-vocalization. PLoS ONE 6:e14744
Greenlee J, Behroozmand R, Etler C, Nourski K, Oya H, Kawasaki H, Howard M (2012) Auditory cortical ECoG findings in a bilateral cochlear implant user during self-vocalization. 4th International Conference on Auditory Cortex. August 31–September 3, 2012, Lausanne, Switzerland, p 142
Hirsh L, Davis H, Silverman S, Reynolds E, Eldert E, Benson R (1952) Development of materials for speech audiometry. J Speech Hear Disord 17:321–337
Howard MA, Volkov IO, Mirsky R, Garell PC, Noh MD, Granner M, Damasio H, Steinschneider M, Reale RA, Hind JE, Brugge JF (2000) Auditory cortex on the human posterior superior temporal gyrus. J Comp Neurol 416:79–92
Howard MA, Nourski KV, Brugge JF (2012) Invasive research methods. In: Fay RR, Popper AN (eds) Springer handbook of auditory research—human auditory cortex. Springer, New York, pp 39–67
Irvine DR, Fallon JB, Kamke MR (2006) Plasticity in the adult central auditory system. Acoust Aust 34:13–17
Jordan K, Schmidt A, Plotz K, von Specht H, Begall K, Roth N, Scheich H (1997) Auditory event-related potentials in post- and prelingually deaf cochlear implant recipients. Am J Otol 18:S116–S117
Kelly AS, Purdy SC, Thorne PR (2005) Electrophysiological and speech perception measures of auditory processing in experienced adult cochlear implant users. Clin Neurophysiol 116:1235–1246
Klinke R, Kral A, Heid S, Tillein J, Hartmann R (1999) Recruitment of the auditory cortex in congenitally deaf cats by long-term cochlear electrostimulation. Science 285:1729–1733
Klinke R, Hartmann R, Heid S, Tillein J, Kral A (2001) Plastic changes in the auditory cortex of congenitally deaf cats following cochlear implantation. Audiol Neurootol 6:203–206
Kral A, Sharma A (2012) Developmental neuroplasticity after cochlear implantation. Trends Neurosci 35:111–122
Kral A, Tillein J (2006) Brain plasticity under cochlear implant stimulation. Adv Otorhinolaryngol 64:89–108
Kral A, Hartmann R, Tillein J, Heid S, Klinke R (2001) Delayed maturation and sensitive periods in the auditory cortex. Audiol Neurootol 6:346–362
Kral A, Hartmann R, Tillein J, Heid S, Klinke R (2002) Hearing after congenital deafness: central auditory plasticity and sensory deprivation. Cereb Cortex 12:797–807
Kral A, Tillein J, Heid S, Hartmann R, Klinke R (2005) Postnatal cortical development in congenital auditory deprivation. Cereb Cortex 15:552–562
Kral A, Tillein J, Hubka P, Schiemann D, Heid S, Hartmann R, Engel AK (2009) Spatiotemporal patterns of cortical activity with bilateral cochlear implants in congenital deafness. J Neurosci 29:811–827
Krueger B, Joseph G, Rost U, Strauss-Schier A, Lenarz T, Buechner A (2008) Performance groups in adult cochlear implant users: speech perception results from 1984 until today. Otol Neurotol 29:509–512
Law SK, Nunez PL, Wijesinghe RS (1993) High-resolution EEG using spline generated surface Laplacians on spherical and ellipsoidal surfaces. IEEE Trans Biomed Eng 40:145–153
Linthicum FH Jr, Anderson W (1991) Cochlear implantation of totally deaf ears. Histologic evaluation of candidacy. Acta Otolaryngol 111:327–31
Linthicum FH Jr, Fayad J, Otto SR, Galey FR, House WF (1991) Cochlear implant histopathology. Am J Otol 12:245–311
Lomber SG, Meredith MA, Kral A (2010) Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf. Nat Neurosci 13:1421–1427
Martin BA (2007) Can the acoustic change complex be recorded in an individual with a cochlear implant? Separating neural responses from cochlear implant artifact. J Am Acad Audiol 18:126–140
McKay CM, McDermott HJ, Clark GM (1994) Pitch percepts associated with amplitude-modulated current pulse trains in cochlear implantees. J Acoust Soc Am 96:2664–2673
Micco AG, Kraus N, Koch DB, McGee TJ, Carrell TD, Sharma A, Nicol T, Wiet RJ (1995) Speeech evoked cognitive p300 potentials in cochlear implant recipients. Am J Otol 16:514–520
Millman RE, Prendergast G, Hymers M, Green GG (2013) Representations of the temporal envelope of sounds in human auditory cortex: can the results from invasive intracortical “depth” electrode recordings be replicated using non-invasive MEG “virtual electrodes”? Neuroimage 64:185–196
Moore DR, Shannon RV (2009) Beyond cochlear implants: awakening the deafened brain. Nat Neurosci 12:686–691
Näätänen R, Picton T (1987) The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology 24:375–425
Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1–25
NIDCD (2011) NIDCD fact sheet: cochlear implants. NIH Publication No. 11-4798
NIH (1995) Cochlear implants in adults and children. NIH Consensus Statement 13:1–30
Nilsson M, Soli SD, Sullivan JA (1994) Development of the hearing in noise test for the measurement of speech reception thresholds in quiet and noise. J Acoust Soc Am 95:1085–1099
Nourski KV, Brugge JF (2011) Representation of temporal sound features in the human auditory cortex. Rev Neurosci 22:187–203
Nourski KV, Oya H, Kawasaki H, Reale RA, Howard MA, Brugge JF (2008) Representation of time-compressed speech in human auditory cortex. Society for Neuroscience 38th Annual Meeting. November 15–19, 2008, Washington, DC Program No. 566.5. 2008 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2008. Online
Nourski KV, Reale RA, Oya H, Kawasaki H, Kovach CK, Chen H, Howard MA III, Brugge JF (2009) Temporal envelope of time-compressed speech represented in the human auditory cortex. J Neurosci 29:15564–15574
Nourski K, Brugge J, Reale R, Oya H, Kawasaki H, Howard M (2010) Electrophysiological study of responses to amplitude-modulated noise within human lateral superior temporal gyrus. Assoc. Res. Otolaryngol. 2010 MidWinter Meeting. February 6–10, 2010, Anaheim, CA. Assoc Res Otolaryngol Abs: 301
Nourski K, Etler C, Brugge J, Oya H, Kawasaki H, Abbas P, Brown C, Howard M (2012) Direct recordings from the auditory cortex in a bilateral cochlear implant user. 4th International Conference on Auditory Cortex. August 31–September 3, 2012, Lausanne, Switzerland, p 140
Nourski KV, Brugge JF, Reale RA, Kovach CK, Kawasaki H, Oya H, Jenison RL, Howard M (2013a) Coding of repetitive transients by auditory cortex on posterolateral superior temporal gyrus in humans: an intracranial electrophysiology study. J Neurophysiol 109:1283–1295
Nourski KV, Steinschneider M, Oya H, Kawasaki H, Jones RD, Howard MA III (2013b) Spectral organization of the human lateral superior temporal gyrus revealed by intracranial recordings. Cereb Cortex. doi:10.1093/cercor/bhs314
Nunez P (1981) Electric fields of the brain. Oxford University Press, New York
Nunez PL, Pilgreen KL (1991) The spline-Laplacian in clinical neurophysiology: a method to improve EEG spatial resolution. J Clin Neurophysiol 8:397–413
Oya H, Kawasaki H, Howard MA III, Adolphs R (2002) Electrophysiological responses in the human amygdala discriminate emotion categories of complex visual stimuli. J Neurosci 22:9502–9512
Pantev C, Ross B, Wollbrink A, Riebandt M, Delank KW, Seifert E, Lamprecht-Dinnesen A (2002) Acoustically and electrically evoked responses of the human cortex before and after cochlear implantation. Hear Res 171:191–195
Perrin F, Pernier J, Bertrand O, Giard MH, Echallier JF (1987) Mapping of scalp potentials by surface spline interpolation. Electroencephalogr Clin Neurophysiol 66:75–81
Ponton CW, Eggermont JJ (2001) Of kittens and kids: altered cortical maturation following profound deafness and cochlear implant use. Audiol Neurootol 6:363–380
Ponton CW, Don M, Eggermont JJ, Waring MD, Masuda A (1996) Maturation of human cortical auditory function: differences between normal-hearing children and children with cochlear implants. Ear Hear 17:430–437
Ponton CW, Moore JK, Eggermont JJ (1999) Prolonged deafness limits auditory system developmental plasticity: evidence from an evoked potentials study in children with cochlear implants. Scand Audiol Suppl 51:13–22
Reale RA, Calvert GA, Thesen T, Jenison RL, Kawasaki H, Oya H, Howard MA, Brugge JF (2007) Auditory–visual processing represented in the human superior temporal gyrus. Neuroscience 145:162–184
Rhone A, Oya H, McMurray B, Reale R, Etler C, Nourski K, Kawasaki H, Howard M (2012) Auditory, visual, and audiovisual speech responses recorded directly from the temporal lobe of a bilateral cochlear implant user. 4th International Conference on Auditory Cortex. August 31–September 3, 2012, Lausanne, Switzerland. p 141
Sandmann P, Plotz K, Volpert S, Siegel M, Schoenfield R, Debener S (2012) Dynamics of cortical plasticity in cochlear-implant users: a prospective longitudinal study. 4th International Conference on Auditory Cortex. August 31–September 3, 2012, Lausanne, Switzerland. p 117
Shannon RV (2007) Understanding hearing through deafness. Proc Nat Acad Sci U S A 104:6883–6884
Shepherd RK, Hardie NA (2001) Deafness-induced changes in the auditory pathway: implications for cochlear implants. Audiol Neurootol 6:305–318
Singh S, Liasis A, Rajput K, Luxon L (2004) Short report: methodological considerations in recording mismatch negativity in cochlear implant patients. Cochlear Implants Int 5:76–80
Steinschneider M, Nourski KV, Kawasaki H, Oya H, Brugge JF, Howard MA III (2011) Intracranial study of speech-elicited activity on the human posterolateral superior temporal gyrus. Cereb Cortex 21:2332–2347
Tillman TW, Carhart R (1966) An expanded test for speech discrimination utilizing CNC monosyllabic words. Northwestern University auditory test No. 6. USAF School of Aerospace Medicine, Brooks Air Force Base, TX
Ventry IM, Weinstein BE (1982) The hearing handicap inventory for the elderly: a new tool. Ear Hear 3:128–134
Viola FC, De Vos M, Hine J, Sandmann P, Bleeck S, Eyles J, Debener S (2012) Semi-automatic attenuation of cochlear implant artifacts for the evaluation of late auditory evoked potentials. Hear Res 284:6–15
Vollmer M, Beitel RE (2011) Behavioral training restores temporal processing in auditory cortex of long-deaf cats. J Neurophysiol 106:2423–2436
Wilson BS, Dorman MF (2009) The design of cochlear implants. In: Niparko JK (ed) Cochlear implants: principles & practices. Lippincott Williams & Wilkins, Philadelphia, pp 95–135
Acknowledgments
We are indebted to our patient for making this work possible. We thank Haiming Chen, Rachel Gold, and Christopher Kovach for their help with data collection and analysis and Pascale Sandmann and Mitchell Steinschneider for their helpful comments. This study was supported by the National Institute on Deafness and Other Communication Disorders at the National Institutes of Health (grant number R01-DC04290), National Center for Research Resources and the National Center for Advancing Translational Sciences at the National Institutes of Health (grant number UL1RR024979), Hearing Health Foundation (Collette Ramsey Baker Award), and the Hoover Fund.
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Nourski, K.V., Etler, C.P., Brugge, J.F. et al. Direct Recordings from the Auditory Cortex in a Cochlear Implant User. JARO 14, 435–450 (2013). https://doi.org/10.1007/s10162-013-0382-3
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DOI: https://doi.org/10.1007/s10162-013-0382-3