Auditory cortex phase locking to amplitude-modulated cochlear implant pulse trains.

Cochlear implant speech processors transmit temporal features of sound as amplitude modulation of constant-rate electrical pulse trains. This study evaluated the central representation of amplitude modulation in the form of phase-locked firing of neurons in the auditory cortex. Anesthetized pigmented guinea pigs were implanted with cochlear electrode arrays. Stimuli were 254 pulse/s (pps) trains of biphasic electrical pulses, sinusoidally modulated with frequencies of 10-64 Hz and modulation depths of -40 to -5 dB re 100% (i.e., 1-56.2% modulation). Single- and multiunit activity was recorded from multi-site silicon-substrate probes. The maximum frequency for significant phase locking (limiting modulation frequency) was >or=60 Hz for 42% of recording sites, whereas phase locking to pulses of unmodulated pulse trains rarely exceeded 30 pps. The strength of phase locking to frequencies >or=40 Hz often varied nonmonotonically with modulation depth, commonly peaking at modulation depths around -15 to -10 dB. Cortical phase locking coded modulation frequency reliably, whereas a putative rate code for frequency was confounded by rate changes with modulation depth. Group delay computed from the slope of mean phase versus modulation frequency tended to increase with decreasing limiting modulation frequency. Neurons in cortical extragranular layers had lower limiting modulation frequencies than did neurons in thalamic afferent layers. Those observations suggest that the low-pass characteristic of cortical phase locking results from intracortical filtering mechanisms. The results show that cortical neurons can phase lock to modulated electrical pulse trains across the range of modulation frequencies and depths presented by cochlear implant speech processors.

[1]  John C Middlebrooks Cochlear-implant high pulse rate and narrow electrode configuration impair transmission of temporal information to the auditory cortex. , 2008, Journal of neurophysiology.

[2]  G. Stickney,et al.  On the dichotomy in auditory perception between temporal envelope and fine structure cues. , 2004, The Journal of the Acoustical Society of America.

[3]  C. Schreiner,et al.  Representation of amplitude modulation in the auditory cortex of the cat. II. Comparison between cortical fields , 1988, Hearing Research.

[4]  Qian-Jie Fu,et al.  Effects of Stimulation Rate, Mode and Level on Modulation Detection by Cochlear Implant Users , 2005, Journal of the Association for Research in Otolaryngology.

[5]  J. Ostwald,et al.  Temporal Coding of Amplitude and Frequency Modulation in the Rat Auditory Cortex , 1995, The European journal of neuroscience.

[6]  Bryan E Pfingst,et al.  Effects of carrier pulse rate and stimulation site on modulation detection by subjects with cochlear implants. , 2007, The Journal of the Acoustical Society of America.

[7]  Alan R Palmer,et al.  Phase-locked responses to pure tones in the primary auditory cortex , 2002, Hearing Research.

[8]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[9]  Hong-Bo Zhao,et al.  Temporal encoding and transmitting of amplitude and frequency modulations in dorsal cochlear nucleus , 1997, Hearing Research.

[10]  B. Delgutte,et al.  Auditory nerve fiber responses to electric stimulation: modulated and unmodulated pulse trains. , 2001, The Journal of the Acoustical Society of America.

[11]  Steven M. Bierer,et al.  Multi-channel spike detection and sorting using an array processing technique , 1999, Neurocomputing.

[12]  M. Semple,et al.  Transformation of Temporal Properties between Auditory Midbrain and Cortex in the Awake Mongolian Gerbil , 2007, The Journal of Neuroscience.

[13]  John C Middlebrooks,et al.  Auditory cortical images of cochlear-implant stimuli: dependence on electrode configuration. , 2002, Journal of neurophysiology.

[14]  Li Xu,et al.  Spectral and temporal cues for phoneme recognition in noise. , 2007, The Journal of the Acoustical Society of America.

[15]  D J Van Tasell,et al.  Speech waveform envelope cues for consonant recognition. , 1987, The Journal of the Acoustical Society of America.

[16]  N. Viemeister Temporal modulation transfer functions based upon modulation thresholds. , 1979, The Journal of the Acoustical Society of America.

[17]  X Wang,et al.  Temporal discharge patterns evoked by rapid sequences of wide- and narrowband clicks in the primary auditory cortex of cat. , 2000, Journal of neurophysiology.

[18]  M Pelizzone,et al.  Low-pass filtering in amplitude modulation detection associated with vowel and consonant identification in subjects with cochlear implants. , 1994, The Journal of the Acoustical Society of America.

[19]  J J Eggermont,et al.  The Magnitude and Phase of Temporal Modulation Transfer Functions in Cat Auditory Cortex , 1999, The Journal of Neuroscience.

[20]  Jos J. Eggermont,et al.  Stimulus induced and spontaneous rhythmic firing of single units in cat primary auditory cortex , 1992, Hearing Research.

[21]  J. Eggermont,et al.  Autonomous cortical rhythms affect temporal modulation transfer functions , 1997, Neuroreport.

[22]  S. Rosen Temporal information in speech: acoustic, auditory and linguistic aspects. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[23]  C. Schreiner,et al.  Representation of amplitude modulation in the auditory cortex of the cat. I. The anterior auditory field (AAF) , 1986, Hearing Research.

[24]  J. Eggermont Temporal modulation transfer functions for AM and FM stimuli in cat auditory cortex. Effects of carrier type, modulating waveform and intensity , 1994, Hearing Research.

[25]  Alan V. Oppenheim,et al.  Discrete-Time Signal Pro-cessing , 1989 .

[26]  Xiaoqin Wang,et al.  Temporal and rate representations of time-varying signals in the auditory cortex of awake primates , 2001, Nature Neuroscience.

[27]  R. Shannon Temporal modulation transfer functions in patients with cochlear implants. , 1992, The Journal of the Acoustical Society of America.

[28]  John C. Middlebrooks,et al.  Directional sensitivity of neurons in the primary auditory (AI) cortex: effects of sound-source intensity level. , 2003, Journal of neurophysiology.

[29]  Fan-Gang Zeng,et al.  Temporal pitch in electric hearing , 2002, Hearing Research.

[30]  G M Clark,et al.  The perception of temporal modulations by cochlear implant patients. , 1993, The Journal of the Acoustical Society of America.

[31]  Bryan E Pfingst,et al.  Relative contributions of spectral and temporal cues for phoneme recognition. , 2005, The Journal of the Acoustical Society of America.

[32]  Bryan E Pfingst,et al.  Features of stimulation affecting tonal-speech perception: implications for cochlear prostheses. , 2002, The Journal of the Acoustical Society of America.

[33]  Xiaoqin Wang,et al.  Neural representations of sinusoidal amplitude and frequency modulations in the primary auditory cortex of awake primates. , 2002, Journal of neurophysiology.

[34]  Gerald Langner,et al.  Periodicity coding in the auditory system , 1992, Hearing Research.

[35]  U. Mitzdorf,et al.  Functional anatomy of the inferior colliculus and the auditory cortex: current source density analyses of click-evoked potentials , 1984, Hearing Research.

[36]  J. C. Middlebrooks,et al.  Auditory Prosthesis with a Penetrating Nerve Array , 2007, Journal for the Association for Research in Otolaryngology.

[37]  R V Shannon,et al.  Speech Recognition with Primarily Temporal Cues , 1995, Science.

[38]  K. Mardia Statistics of Directional Data , 1972 .

[39]  H J McDermott,et al.  Pitch percepts associated with amplitude-modulated current pulse trains in cochlear implantees. , 1994, The Journal of the Acoustical Society of America.

[40]  C E Schreiner,et al.  Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation. II. Repetition rate coding. , 1996, Journal of neurophysiology.

[41]  M. Semple,et al.  Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. , 2000, Journal of neurophysiology.

[42]  R. Plomp,et al.  Effect of temporal envelope smearing on speech reception. , 1994, The Journal of the Acoustical Society of America.

[43]  L Geurts,et al.  Coding of the fundamental frequency in continuous interleaved sampling processors for cochlear implants. , 2001, The Journal of the Acoustical Society of America.

[44]  M Steinschneider,et al.  Click train encoding in primary auditory cortex of the awake monkey: evidence for two mechanisms subserving pitch perception. , 1998, The Journal of the Acoustical Society of America.

[45]  D. P. Phillips,et al.  Timing of spike discharges in cat auditory cortex neurons: Implications for encoding of stimulus periodicity , 1989, Hearing Research.

[46]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[47]  M Vollmer,et al.  Responses of inferior colliculus neurons to amplitude-modulated intracochlear electrical pulses in deaf cats. , 2000, Journal of neurophysiology.

[48]  J. Eggermont Temporal modulation transfer functions in cat primary auditory cortex: separating stimulus effects from neural mechanisms. , 2002, Journal of neurophysiology.

[49]  Jos J. Eggermont,et al.  Rate and synchronization measures of periodicity coding in cat primary auditory cortex , 1991, Hearing Research.

[50]  G M Clark,et al.  Modulation detection interference in cochlear implant subjects. , 1998, The Journal of the Acoustical Society of America.

[51]  M. Goldstein,et al.  Intracellular study of the cat's primary auditory cortex. , 1972, Brain research.

[52]  J. Eggermont Representation of spectral and temporal sound features in three cortical fields of the cat. Similarities outweigh differences. , 1998, Journal of neurophysiology.

[53]  J K Shallop,et al.  Evaluation of a new spectral peak coding strategy for the Nucleus 22 Channel Cochlear Implant System. , 1994, The American journal of otology.

[54]  F. Zeng,et al.  Temporal Masking in Electric Hearing , 2006, Journal of the Association for Research in Otolaryngology.

[55]  A. Nuttall,et al.  Effects of perilymphatic perfusion with neomycin on the cochlear microphonic potential in the guinea pig. , 1977, Acta oto-laryngologica.

[56]  R. L. Rennaker,et al.  Response to broadband repetitive stimuli in auditory cortex of the unanesthetized rat , 2006, Hearing Research.

[57]  J. Goldberg,et al.  Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. , 1969, Journal of neurophysiology.

[58]  William M. Rabinowitz,et al.  Better speech recognition with cochlear implants , 1991, Nature.

[59]  C. Schreiner,et al.  Thalamocortical transformation of responses to complex auditory stimuli , 2004, Experimental Brain Research.

[60]  C E Schreiner,et al.  Neural processing of amplitude-modulated sounds. , 2004, Physiological reviews.

[61]  Fan-Gang Zeng,et al.  Music Perception with Temporal Cues in Acoustic and Electric Hearing , 2004, Ear and hearing.

[62]  R. Shannon,et al.  Effect of stimulation rate on phoneme recognition by nucleus-22 cochlear implant listeners. , 2000, The Journal of the Acoustical Society of America.

[63]  A. Rees,et al.  Neuronal responses to amplitude-modulated and pure-tone stimuli in the guinea pig inferior colliculus, and their modification by broadband noise. , 1989, The Journal of the Acoustical Society of America.