Skip to main content

Better Temporal Neural Coding with Cochlear Implants in Awake Animals

  • Conference paper
  • First Online:
Basic Aspects of Hearing

Part of the book series: Advances in Experimental Medicine and Biology ((volume 787))

Abstract

Both the performance of cochlear implant (CI) listeners and the responses of auditory neurons show limits in temporal processing at high frequencies. However, the upper limit of temporal coding of pulse-train stimuli in the inferior colliculus (IC) of anesthetized animals appears to be lower than that observed in corresponding perceptual tasks. We hypothesize that the neural rate limits have been underestimated due to the effect of anesthesia. To test this hypothesis, we developed a chronic, awake rabbit preparation for recording responses of single IC neurons to CI stimulation without the confound of anesthesia and compared these data with earlier recordings from the IC of anesthetized cats. Stimuli were periodic trains of biphasic pulses with rates varying from 20 to 1,280 pulses per second (pps). We found that the maximum pulse rates that elicited sustained firing and phase-locked responses were 2–3 times higher in the IC of awake rabbits than in anesthetized cats. Moreover, about 25 % of IC neurons in awake rabbit showed sustained responses to periodic pulse trains at much higher pulse rates (>1,000 pps) than observed in anesthetized animals. Similar differences were observed in single units whose responses to pulse trains were monitored while the animal was given an injection of an ultrashort-acting anesthetic. In general, the physiological rate limits of IC neurons in awake rabbit are more consistent with the psychophysical limits in human CI subjects compared to the data from anesthetized animals.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Colburn HS, Chung Y, Zhou Y, Brughera A (2009) Models of brainstem responses to bilateral electrical stimulation. J Assoc Res Otolaryngol 10:91–110

    Article  PubMed  Google Scholar 

  • Devore S, Delgutte B (2010) Effects of reverberation on the directional sensitivity of auditory neurons across the tonotopic axis: influences of interaural time and level differences. J Neurosci 30:7826–7837

    Article  PubMed  CAS  Google Scholar 

  • Ebert CS, Fitzpatrick DC, Cullen RD, Finley CC, Bassim MK, Zdanski CJ, Coffey CS, Crocker W, Skaggs J, Marshall AF, Falk SE (2004) Responses of binaural neurons to combined auditory and electrical stimulation. Abstr Assoc Res Otolaryngol 27:485

    Google Scholar 

  • Hancock KE, Noel V, Ryugo DK, Delgutte B (2010) Neural coding of interaural time differences with bilateral cochlear implants: effects of congenital deafness. J Neurosci 30:14068–14079

    Article  PubMed  CAS  Google Scholar 

  • Hancock KE, Chung Y, Delgutte B (2012) Neural ITD coding with bilateral cochlear implants: effect of binaurally-coherent jitter. J Neurophysiol 108:714–728

    Article  PubMed  Google Scholar 

  • Hara K, Harris RA (2002) The anesthetic mechanism of urethane: the effects on neurotransmitter-gated ion channels. Anesth Analg 94:313–318

    PubMed  CAS  Google Scholar 

  • Johnson L, Santina CD, Wang X (2011) Neural responses to cochlear implant stimulation in auditory cortex of awake marmoset. Abstr Assoc Res Otolaryngol 34:943

    Google Scholar 

  • Kirby AE, Middlebrooks JC (2012) Unanesthetized auditory cortex exhibits multiple codes for gaps in cochlear implant pulse trains. J Assoc Res Otolaryngol 13:67–80

    Article  PubMed  Google Scholar 

  • Kuwada S, Batra R, Stanford TR (1989) Monaural and binaural response properties of neurons in the inferior colliculus of the rabbit: effects of sodium pentobarbital. J Neurophysiol 61:269–282

    PubMed  CAS  Google Scholar 

  • Manis PB, Marx SO (1991) Outward currents in isolated ventral cochlear nucleus neurons. J Neurosci 11:2865–2880

    PubMed  CAS  Google Scholar 

  • Smith ZM, Delgutte B (2007) Sensitivity to interaural time differences in the inferior colliculus with bilateral cochlear implants. J Neurosci 27:6740– 6750

    PubMed  CAS  Google Scholar 

  • Snyder R, Leake P, Rebscher S, Beitel R (1995) Temporal resolution of neurons in cat inferior ­colliculus to intracochlear electrical stimulation: effects of neonatal deafening and chronic stimulation. J Neurophysiol 73:449–467

    PubMed  CAS  Google Scholar 

  • Ter-Mikaelian M, Sanes DH, Semple MN (2007) Transformation of temporal properties between auditory midbrain and cortex in the awake Mongolian gerbil. J Neurosci 27:6091–6102

    Article  PubMed  CAS  Google Scholar 

  • Tong YC, Clark GM (1985) Absolute identification of electric pulse rates and electrode positions by cochlear implant patients. J Acoust Soc Am 77:1881–1888

    Article  PubMed  CAS  Google Scholar 

  • Townshend B, Cotter N, Compernolle D, White RL (1987) Pitch perception by cochlear implant subjects. J Acoust Soc Am 82:106–115

    Article  PubMed  CAS  Google Scholar 

  • van Hoesel RJ (2007) Sensitivity to binaural timing in bilateral cochlear implant users. J Acoust Soc Am 121:2192–2206

    Article  PubMed  Google Scholar 

  • Werz MA, Macdonald RL (1985) Barbiturates decrease voltage-dependent calcium conductance of mouse neurons in dissociated cell culture. Mol Pharmacol 28:269–277

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Supported by NIH grants R01DC005775 and P30DC005209, Curing Kids Fund from Massachusetts Eye and Ear and a Hearing Health Foundation grant to Y. Chung. We thank Connie Miller, Melissa McKinnon, and Mike Kaplan for technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yoojin Chung PhD .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this paper

Cite this paper

Chung, Y., Hancock, K.E., Nam, SI., Delgutte, B. (2013). Better Temporal Neural Coding with Cochlear Implants in Awake Animals. In: Moore, B., Patterson, R., Winter, I., Carlyon, R., Gockel, H. (eds) Basic Aspects of Hearing. Advances in Experimental Medicine and Biology, vol 787. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-1590-9_39

Download citation

Publish with us

Policies and ethics