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Neural Mechanisms Supporting Robust Discrimination of Spectrally and Temporally Degraded Speech

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Abstract

Cochlear implants provide good speech discrimination ability despite highly limited amount of information they transmit compared with normal cochlea. Noise vocoded speech, simulating cochlear implants in normal hearing listeners, have demonstrated that spectrally and temporally degraded speech contains sufficient cues to provide accurate speech discrimination. We hypothesized that neural activity patterns generated in the primary auditory cortex by spectrally and temporally degraded speech sounds will account for the robust behavioral discrimination of speech. We examined the behavioral discrimination of noise vocoded consonants and vowels by rats and recorded neural activity patterns from rat primary auditory cortex (A1) for the same sounds. We report the first evidence of behavioral discrimination of degraded speech sounds by an animal model. Our results show that rats are able to accurately discriminate both consonant and vowel sounds even after significant spectral and temporal degradation. The degree of degradation that rats can tolerate is comparable to human listeners. We observed that neural discrimination based on spatiotemporal patterns (spike timing) of A1 neurons is highly correlated with behavioral discrimination of consonants and that neural discrimination based on spatial activity patterns (spike count) of A1 neurons is highly correlated with behavioral discrimination of vowels. The results of the current study indicate that speech discrimination is resistant to degradation as long as the degraded sounds generate distinct patterns of neural activity.

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References

  • Anderson SE, Kilgard MP, Sloan AM, Rennaker RL (2006) Response to broadband repetitive stimuli in auditory cortex of the unanesthetized rat. Hearing Res 213:107–117

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Boemio A, Fromm S, Braun A, Poeppel D (2005) Hierarchical and asymmetric temporal sensitivity in human auditory cortices. Nat Neurosci 8:389–395

    Article  PubMed  CAS  Google Scholar 

  • Britten KH, Shadlen MN, Newsome WT, Movshon JA (1992) The analysis of visual motion: a comparison of neuronal and psychophysical performance. The J of neurosci: the Off J of the Soc for Neurosci 12:4745–4765

    CAS  Google Scholar 

  • Buonomano DV, Merzenich MM (1995) Temporal information transformed into a spatial code by a neural-network with realistic properties. Science 267:1028–1030

    Article  PubMed  CAS  Google Scholar 

  • Buonomano DV, Merzenich M (1999) A neural network model of temporal code generation and position-invariant pattern recognition. Neural Comput 11:103–116

    Article  PubMed  CAS  Google Scholar 

  • Christensen TA, Antonucci SM, Lockwood JL, Kittleson M, Plante E (2008) Cortical and subcortical contributions to the attentive processing of speech. Neuroreport 19:1101–1105

    Article  PubMed  Google Scholar 

  • 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. Hearing Res 169:97–111

    Article  Google Scholar 

  • Davis MH, Johnsrude IS (2003) Hierarchical processing in spoken language comprehension. J of Neurosci J Soc Neurosci 23:3423–3431

    CAS  Google Scholar 

  • Delgutte B, Kiang NY (1984) Speech coding in the auditory nerve: I. Vowel-like sounds. J Acoust Soc Am 75:866–878

    Article  PubMed  CAS  Google Scholar 

  • Dorman MF, Loizou PC (1997) Speech intelligibility as a function of the number of channels of stimulation for normal-hearing listeners and patients with cochlear implants. Am J Otol 18:S113–S114

    PubMed  CAS  Google Scholar 

  • Dorman MF, Loizou PC, Fitzke J, Tu Z (1998) The recognition of sentences in noise by normal-hearing listeners using simulations of cochlear-implant signal processors with 6–20 channels. J Acoust Soc Am 104:3583–3585

    Article  PubMed  CAS  Google Scholar 

  • Drullman R, Festen JM, Plomp R (1994) Effect of temporal envelope smearing on speech reception. J Acoust Soc Am 95:1053–1064

    Article  PubMed  CAS  Google Scholar 

  • Engineer CT, Perez CA, Chen YTH, Carraway RS, Reed AC, Shetake JA, Jakkamsetti V, Chang KQ, Kilgard MP (2008) Cortical activity patterns predict speech discrimination ability. Nat Neurosci 11:603–608

    Article  PubMed  CAS  Google Scholar 

  • Fishman KE, Shannon RV, Slattery WH (1997) Speech recognition as a function of the number of electrodes used in the SPEAK cochlear implant speech processor. J Speech Lang Hear R 40:1201–1215

    CAS  Google Scholar 

  • Foffani G, Moxon KA (2004) PSTH-based classification of sensory stimuli using ensembles of single neurons. J Neurosci Meth 135:107–120

    Article  Google Scholar 

  • Gatehouse S (1992) The time course and magnitude of perceptual acclimatization to frequency responses: evidence from monaural fitting of hearing aids. J Acoust Soc Am 92:1258–1268

    Article  PubMed  CAS  Google Scholar 

  • Grady CL, Van Meter JW, Maisog JM, Pietrini P, Krasuski J, Rauschecker JP (1997) Attention-related modulation of activity in primary and secondary auditory cortex. Neuroreport 8:2511–2516

    Article  PubMed  CAS  Google Scholar 

  • Green DM, Swets JA (1989) Signal detection theory and psychophysics. Los Altos, CA: Peninsula Publishing

  • Hedrick MS, Carney AE (1997) Effect of relative amplitude rind formant transitions on perception of place of articulation by adult listeners with cochlear implants. J Speech Lang Hear R 40:1445–1457

    CAS  Google Scholar 

  • Hugdahl K, Thomsen T, Ersland L, Rimol LM, Niemi J (2003) The effects of attention on speech perception: an fMRI study. Brain Lang 85:37–48

    Article  PubMed  Google Scholar 

  • Hughes ML, Vander Werff KR, Brown CJ, Abbas PJ, Kelsay DM, Teagle HF, Lowder MW (2001) A longitudinal study of electrode impedance, the electrically evoked compound action potential, and behavioral measures in nucleus 24 cochlear implant users. Ear Hear 22:471–486

    Article  PubMed  CAS  Google Scholar 

  • Kawahara H (1997) Speech representation and transformation using adaptive interpolation of weighted spectrum. IEEE Trans Acoust Speech Sig Process 2:1303–1306

    Google Scholar 

  • Kiefer J, von Ilberg C, Rupprecht V, Hubner-Egner J, Knecht R (2000) Optimized speech understanding with the continuous interleaved sampling speech coding strategy in patients with cochlear implants: effect of variations in stimulation rate and number of channels. Ann Otol Rhinol Laryngol 109:1009–1020

    PubMed  CAS  Google Scholar 

  • Kilgard MP, Merzenich MM (1998) Cortical map reorganization enabled by nucleus basalis activity. Science 279:1714–1718

    Article  PubMed  CAS  Google Scholar 

  • Kral A (2007) Unimodal and cross-modal plasticity in the ‘deaf’ auditory cortex. Int J Audiol 46:479–493

    Article  PubMed  Google Scholar 

  • Kral A, Tillein J (2006) Brain plasticity under cochlear implant stimulation. Adv Otorhinolaryngol 64:89–108

    PubMed  Google Scholar 

  • Kral A, Tillein J, Heid S, Klinke R, Hartmann R (2006) Cochlear implants: cortical plasticity in congenital deprivation. Prog Brain Res 157:283–313

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Kumar A, Rotter S, Aertsen A (2010) Spiking activity propagation in neuronal networks: reconciling different perspectives on neural coding. Nat Rev Neurosci 11:615–627

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Newsome WT (2005) Correlation between speed perception and neural activity in the middle temporal visual area. The Journal of neuroscience: the official journal of the Society for Neuroscience 25:711–722

    Article  CAS  Google Scholar 

  • Loebach JL, Wickesberg RE (2006) The representation of noise vocoded speech in the auditory nerve of the chinchilla: physiological correlates of the perception of spectrally reduced speech. Hearing Res 213:130–144

    Article  Google Scholar 

  • Loizou PC (1998) Mimicking the human ear. Ieee Signal Proc Mag 15:101–130

    Article  Google Scholar 

  • Loizou PC (2006) Speech processing in vocoder-centric cochlear implants. Adv Otorhinolaryngol 64:109–143

    PubMed  Google Scholar 

  • Loizou PC, Dorman M, Tu ZM (1999) On the number of channels needed to understand speech. J Acoust Soc Am 106:2097–2103

    Article  PubMed  CAS  Google Scholar 

  • Loizou PC, Poroy O, Dorman M (2000) The effect of parametric variations of cochlear implant processors on speech understanding. J Acoust Soc Am 108:790–802

    Article  PubMed  CAS  Google Scholar 

  • Mauk MD, Buonomano DV (2004) The neural basis of temporal processing. Annu Rev Neurosci 27:307–340

    Article  PubMed  CAS  Google Scholar 

  • Moore DR, Shannon RV (2009) Beyond cochlear implants: awakening the deafened brain. Nat Neurosci 12:686–691

    Article  PubMed  CAS  Google Scholar 

  • Nie K, Barco A, Zeng FG (2006) Spectral and temporal cues in cochlear implant speech perception. Ear Hear 27:208–217

    Article  PubMed  Google Scholar 

  • Ohl FW, Scheich H (1997) Orderly cortical representation of vowels based on formant interaction. P Natl Acad Sci U S A 94:9440–9444

    Article  CAS  Google Scholar 

  • Panzeri S, Brunel N, Logothetis NK, Kayser C (2010) Sensory neural codes using multiplexed temporal scales. Trends Neurosci 33:111–120

    Article  PubMed  CAS  Google Scholar 

  • Perez CA, Engineer CT, Jakkamsetti V, Carraway RS, Perry MS, Kilgard MP (2012) Different time scales for the neural coding of consonant and vowel sounds. New York, NY: Cereb Cortex

  • Peterson G, Barney H (1952) Control methods used in a study of the vowels. J Acoust Soc Am 24:175–183

    Article  Google Scholar 

  • Poeppel D (2003) The analysis of speech in different temporal integration windows: cerebral lateralization as ‘asymmetric sampling in time’. Speech Commun 41:245–255

    Article  Google Scholar 

  • Rao D, Basura GJ, Roche J, Daniels S, Mancilla JG, Manis PB (2010) Hearing loss alters serotonergic modulation of intrinsic excitability in auditory cortex. J Neurophysiol 104:2693–2703

    Article  PubMed  Google Scholar 

  • Rennaker RL, Carey HL, Anderson SE, Sloan AM, Kilgard MP (2007) Anesthesia suppresses nonsynchronous responses to repetitive broadband stimuli. Neuroscience 145:357–369

    Article  PubMed  CAS  Google Scholar 

  • Romo R, Salinas E (2003) Flutter discrimination: neural codes, perception, memory and decision making. Nat Rev Neurosci 4:203–218

    Article  PubMed  CAS  Google Scholar 

  • Sachs MB, Young ED (1979) Encoding of steady-state vowels in the auditory nerve: representation in terms of discharge rate. J Acoust Soc Am 66:470–479

    Article  PubMed  CAS  Google Scholar 

  • Scott SK, Blank CC, Rosen S, Wise RJ (2000) Identification of a pathway for intelligible speech in the left temporal lobe. Brain 123(Pt 12):2400–2406

    Article  PubMed  Google Scholar 

  • Scott SK, Rosen S, Lang H, Wise RJ (2006) Neural correlates of intelligibility in speech investigated with noise vocoded speech—a positron emission tomography study. J Acoust Soc Am 120:1075–1083

    Article  PubMed  Google Scholar 

  • Shannon RV, Zeng FG, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primarily temporal cues. Science 270:303–304

    Article  PubMed  CAS  Google Scholar 

  • Sharma A, Gilley PM, Dorman MF, Baldwin R (2007) Deprivation-induced cortical reorganization in children with cochlear implants. Int J Audiol 46:494–499

    Article  PubMed  Google Scholar 

  • Shetake JA, Wolf JT, Cheung RJ, Engineer CT, Ram SK, Kilgard MP (2011) Cortical activity patterns predict robust speech discrimination ability in noise. Eur J Neurosci 34:1823–1838

    Article  PubMed  Google Scholar 

  • Sinex DG, Chen GD (2000) Neural responses to the onset of voicing are unrelated to other measures of temporal resolution. J Acoust Soc Am 107:486–495

    Article  PubMed  CAS  Google Scholar 

  • Steinschneider M, Arezzo J, Vaughan HG Jr (1982) Speech evoked activity in the auditory radiations and cortex of the awake monkey. Brain Res 252:353–365

    Article  PubMed  CAS  Google Scholar 

  • Steinschneider M, Volkov IO, Noh MD, Garell PC, Howard MA 3rd (1999) Temporal encoding of the voice onset time phonetic parameter by field potentials recorded directly from human auditory cortex. J Neurophysiol 82:2346–2357

    PubMed  CAS  Google Scholar 

  • Steinschneider M, Fishman YI, Arezzo JC (2003) Representation of the voice onset time (VOT) speech parameter in population responses within primary auditory cortex of the awake monkey. J Acoust Soc Am 114:307–321

    Article  PubMed  Google Scholar 

  • Steinschneider M, Volkov IO, Fishman YI, Oya H, Arezzo JC, Howard MA 3rd (2005) Intracortical responses in human and monkey primary auditory cortex support a temporal processing mechanism for encoding of the voice onset time phonetic parameter. Cereb Cortex 15:170–186

    Article  PubMed  Google Scholar 

  • Tyler RS, Summerfield AQ (1996) Cochlear implantation: relationships with research on auditory deprivation and acclimatization. Ear Hear 17:38S–50S

    Article  PubMed  CAS  Google Scholar 

  • Valimaa TT, Maatta TK, Lopponen HJ, Sorri MJ (2002) Phoneme recognition and confusions with multichannel cochlear implants: consonants. J Speech Lang Hear Res 45:1055–1069

    Article  PubMed  Google Scholar 

  • Van Tasell DJ, Soli SD, Kirby VM, Widin GP (1987) Speech waveform envelope cues for consonant recognition. J Acoust Soc Am 82:1152–1161

    Article  PubMed  Google Scholar 

  • Versnel H, Shamma SA (1998) Spectral-ripple representation of steady-state vowels in primary auditory cortex. J Acoust Soc Am 103:2502–2514

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T (1978) Responses of the cat’s collicular auditory neuron to human speech. J Acoust Soc Am 64:333–337

    Article  PubMed  CAS  Google Scholar 

  • Won JH, Drennan WR, Rubinstein JT (2007) Spectral-ripple resolution correlates with speech reception in noise in cochlear implant users. J Assoc Res Otolaryngol 8:384–392

    Article  PubMed  Google Scholar 

  • Xu L, Thompson CS, Pfingst BE (2005) Relative contributions of spectral and temporal cues for phoneme recognition. J Acoust Soc Am 117:3255–3267

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank T. R. Rosenthal, E. M. Renfroe, T. K. Jasti, E. Tran, K. Ram, R. Cheung, H. Shepard, Z. Ghneim, C. Xie, D. Vuppula, T. Nguyen, and R. Joseph for help with behavioral training. We would also like to thank, A. Moller, P. Assmann, E. Tobey, F. G. Zeng, C. Engineer, B. Porter, J. Shetake, and A. Reed for their comments and suggestions on earlier versions of the manuscript. We would also like to thank P.C. Loizou in his assistance in signal processing and for his comments and suggestions on the manuscript. We would also like to thank H. Abdi for his guidance in statistical analyses. This work was supported by Award Numbers R01DC010433 and R15DC006624 from the National Institute on Deafness and Other Communication Disorders.

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Correspondence to Kamalini G. Ranasinghe.

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Ranasinghe, K.G., Vrana, W.A., Matney, C.J. et al. Neural Mechanisms Supporting Robust Discrimination of Spectrally and Temporally Degraded Speech. JARO 13, 527–542 (2012). https://doi.org/10.1007/s10162-012-0328-1

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