Neuronal Activity Evoked in the Inferior Colliculus of the Cat by Surface Macroelectrodes and Penetrating Microelectrodes Implanted in the Cochlear Nucleus

Persons lacking functional auditory nerves cannot benefit from cochlear implants, but an auditory brainstem implant (ABI) utilizing stimulating electrodes adjacent to or on their cochlear nucleus (CN) can restore some hearing. We are investigating the feasibility of supplementing these surface electrodes with penetrating microstimulating electrodes within the ventral CN (VCN), and how the two types of electrodes can be used synergistically. Multiunit neuronal responses evoked by VCN electrical stimulation with surface electrodes and microelectrodes were recorded in the inferior colliculus (ICC) of five cats. The findings are consistent with those from patients with type II neurofibromatosis who received ABIs with both surface and microelectrodes. The patients described percepts from their microelectrodes as more similar to pure tones than those from their surface electrodes, consistent with the greater tonotopic selectivity of microelectrodes in the cats' VCN. Also, the patients describe percepts from their surface electrodes as louder than those from the microelectrodes, while in the cat, the neuronal activity evoked in the ICC by the surface electrodes tended to be greater. This concordance helps to validate our cat model as a means of investigating the synergistic use of surface and penetrating electrodes in a clinical ABI.

[1]  T. Lenarz,et al.  Auditory Brainstem Implant: Part I. Auditory Performance and Its Evolution Over Time , 2001, Otology & neurotology : official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology.

[2]  John K. Niparko,et al.  Direct Electrical Stimulation of the Cochlear Nucleus: Surface vs. Penetrating Stimulation , 1991, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[3]  Y Kim,et al.  Uniformity of current density under stimulating electrodes. , 1990, Critical reviews in biomedical engineering.

[4]  N. Cant,et al.  Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei , 2003, Brain Research Bulletin.

[5]  R. Laszig,et al.  Surgical experiences in 58 cases using the Nucleus 22 multichannel auditory brainstem implant , 2000, The Journal of Laryngology & Otology.

[6]  C. McIntyre,et al.  Finite Element Analysis of the Current-Density and Electric Field Generated by Metal Microelectrodes , 2001, Annals of Biomedical Engineering.

[7]  William S. Rhode,et al.  Temporal coding of 200% amplitude modulated signals in the ventral cochlear nucleus of cat , 1994, Hearing Research.

[8]  C. McIntyre,et al.  Excitation of central nervous system neurons by nonuniform electric fields. , 1999, Biophysical journal.

[9]  Y. Seki [Restoration of hearing--comparing auditory brainstem implant to cochlear implant]. , 2007, Brain and nerve = Shinkei kenkyu no shinpo.

[10]  M. Malmierca,et al.  Laminar inputs from dorsal cochlear nucleus and ventral cochlear nucleus to the central nucleus of the inferior colliculus: Two patterns of convergence , 2005, Neuroscience.

[11]  J M Miller,et al.  Multiple-Channel Stimulation of the Cochlear Nucleus , 1989, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[12]  Stefan J. Mauger,et al.  Inferior colliculus responses to multichannel microstimulation of the ventral cochlear nucleus: implications for auditory brain stem implants. , 2008, Journal of neurophysiology.

[13]  R. Shannon,et al.  Progress in restoration of hearing with the auditory brainstem implant. , 2009, Progress in brain research.

[14]  Martin Han,et al.  A new chronic neural probe with electroplated iridium oxide microelectrodes , 2008, 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[15]  W. S. Rhode,et al.  Encoding of amplitude modulation in the cochlear nucleus of the cat. , 1994, Journal of neurophysiology.

[16]  Robert V. Shannon,et al.  Auditory brainstem implants , 2011, Neurotherapeutics.

[17]  Russell L. Snyder,et al.  Quantitative analysis of spiral ganglion projections to the cat cochlear nucleus , 1997, The Journal of comparative neurology.

[18]  D.B. McCreery,et al.  A characterization of the effects on neuronal excitability due to prolonged microstimulation with chronically implanted microelectrodes , 1997, IEEE Transactions on Biomedical Engineering.

[19]  Shigeto Furukawa,et al.  Auditory Cortical Images of Tones and Noise Bands , 2000, Journal of the Association for Research in Otolaryngology.

[20]  D. McCreery,et al.  Stimulus parameters affecting tissue injury during microstimulation in the cochlear nucleus of the cat , 1994, Hearing Research.

[21]  Russell L. Martin,et al.  The three-dimensional frequency organization of the inferior colliculus of the cat: a 2-deoxyglucose study , 1997, Hearing Research.

[22]  D R Moore,et al.  Inferior colliculus. II. Development of tuning characteristics and tonotopic organization in central nucleus of the neonatal cat. , 1975, Journal of neurophysiology.

[23]  D. McCreery,et al.  Cochlear nucleus auditory prostheses , 2008, Hearing Research.

[24]  J. Zwislocki Cochlear precursors of neural pitch and loudness codes. , 1995, The Annals of otology, rhinology & laryngology. Supplement.

[25]  D.B. McCreery,et al.  Charge density and charge per phase as cofactors in neural injury induced by electrical stimulation , 1990, IEEE Transactions on Biomedical Engineering.

[26]  Robert V Shannon,et al.  Open Set Speech Perception with Auditory Brainstem Implant? , 2005, The Laryngoscope.

[27]  Robert V Shannon,et al.  Multichannel auditory brainstem implant: update on performance in 61 patients. , 2002, Journal of neurosurgery.

[28]  T.L. Rose,et al.  Electrical stimulation with Pt electrodes. VIII. Electrochemically safe charge injection limits with 0.2 ms pulses (neuronal application) , 1990, IEEE Transactions on Biomedical Engineering.

[29]  K K Osen,et al.  The cochlear nuclei in man. , 1979, The American journal of anatomy.

[30]  Victor Pikov,et al.  Performance of Multisite Silicon Microprobes Implanted Chronically in the Ventral Cochlear Nucleus of the Cat , 2007, IEEE Transactions on Biomedical Engineering.

[31]  Graeme M. Clark,et al.  Histological and physiological effects of the central auditory prosthesis: surface versus penetrating electrodes , 1997, Hearing Research.

[32]  Hirokazu Takahashi,et al.  Accessing ampli-tonotopic organization of rat auditory cortex by microstimulation of cochlear nucleus , 2005, IEEE Transactions on Biomedical Engineering.

[33]  M M Merzenich,et al.  Representation of the cochlea within the inferior colliculus of the cat. , 1974, Brain research.

[34]  S K Rosahl,et al.  Far-field responses to stimulation of the cochlear nucleus by microsurgically placed penetrating and surface electrodes in the cat. , 2001, Journal of neurosurgery.

[35]  M. Hallett,et al.  What does the ratio of injected current to electrode area tell us about current density in the brain during tDCS? , 2009, Clinical Neurophysiology.

[36]  M. Merzenich,et al.  Neuronal discharge rate is unsuitable for encoding sound intensity at the inferior-colliculus level , 1988, Hearing Research.

[37]  Brian C J Moore,et al.  Coding of Sounds in the Auditory System and Its Relevance to Signal Processing and Coding in Cochlear Implants , 2003, Otology & neurotology : official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology.

[38]  R V Shannon,et al.  Accessing the tonotopic organization of the ventral cochlear nucleus by intranuclear microstimulation. , 1998, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

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

[40]  N. Cant,et al.  Organization of the inferior colliculus of the gerbil (Meriones unguiculatus): Differences in distribution of projections from the cochlear nuclei and the superior olivary complex , 2006, The Journal of comparative neurology.

[41]  D. McCreery,et al.  Chronic microstimulation in the feline ventral cochlear nucleus: physiologic and histologic effects , 2000, Hearing Research.

[42]  William F. Agnew,et al.  The Effects of Prolonged Intracortical Microstimulation on the Excitability of Pyramidal Tract Neurons in the Cat , 2004, Annals of Biomedical Engineering.

[43]  D. Oliver Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: Possible substrates for binaural interaction , 1987, The Journal of comparative neurology.

[44]  E G Jones,et al.  The neuronal organization of the inferior colliculus of the adult cat. I. The central nucleus , 1973, The Journal of comparative neurology.

[45]  W. S. Rhode,et al.  Encoding timing and intensity in the ventral cochlear nucleus of the cat. , 1986, Journal of neurophysiology.

[46]  R. Shannon,et al.  Outcomes in Nontumor Adults Fitted With the Auditory Brainstem Implant: 10 Years' Experience , 2009, Otology & neurotology : official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology.

[47]  Robert V Shannon,et al.  Audiologic Outcomes With the Penetrating Electrode Auditory Brainstem Implant , 2008, Otology & neurotology : official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology.

[48]  John C. Middlebrooks,et al.  Topographic Spread of Inferior Colliculus Activation in Response to Acoustic and Intracochlear Electric Stimulation , 2004, Journal of the Association for Research in Otolaryngology.