Accessing the tonotopic organization of the ventral cochlear nucleus by intranuclear microstimulation.

This study is part of a program to develop an auditory prosthesis for the profoundly deaf, based on multichannel microstimulation in the cochlear nucleus. The functionality of such a device is dependent on its ability to access the tonotopic axis of the human ventral cochlear nucleus in an orderly fashion. In these studies, we utilized the homologies between the human and feline ventral cochlear nuclei and the known tonotopic organization of the central nucleus of the inferior colliculus (IC). In anesthetized cats, stimuli were delivered to three or four locations along the dorsal-to-ventral axis of the posteroventral cochlear nucleus (PVCN), and for each stimulus location, we recorded the multiunit neuronal activity and the field potentials at 20 or more locations along the dorsolateral-ventromedial (tonotopic) axis of the IC. The current source-sink density (CSD), which delimits regions of neuronal activity, was computed from the sequence of field potentials recorded along this axis. The multiunit activity and the CSD analysis both showed that the tonotopic organization of the PVCN can be accessed in an orderly manner by intranuclear microstimulation in several regions of the PVCN, using the range of stimulus pulse amplitudes that have been shown in previous studies to be noninjurious during prolonged intranuclear microstimulation via chronically implanted microelectrodes. We discuss the applicability of these findings to the design of clinical auditory prostheses for implantation into the human cochlear nucleus.

[1]  Robert V Shannon,et al.  Psychophysical measures from electrical stimulation of the human cochlear nucleus , 1990, Hearing Research.

[2]  Jean K. Moore The human auditory brain stem: A comparative view , 1987, Hearing Research.

[3]  Robert V Shannon,et al.  Threshold functions for electrical stimulation of the human cochlear nucleus , 1989, Hearing Research.

[4]  W M COWAN,et al.  An experimental study of the projection of the cochlea. , 1962, Journal of anatomy.

[5]  I. Sando The Anatomical Interrelationships of the Cochlear Nerve Fibers , 1965 .

[6]  Robert V. Shannon,et al.  Auditory Brainstem Implant: I. Issues in Surgical Implantation , 1993, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[7]  C. Nicholson,et al.  Experimental optimization of current source-density technique for anuran cerebellum. , 1975, Journal of neurophysiology.

[8]  N. Cant Identification of cell types in the anteroventral cochlear nucleus that project to the inferior colliculus , 1982, Neuroscience Letters.

[9]  D. Harris Current source density analysis of frequency coding in the inferior colliculus , 1987, Hearing Research.

[10]  K. Osen,et al.  γ‐aminobutyric acid and glycine in the baboon cochlear nuclei: An immunocytochemical colocalization study with reference to interspecies differences in inhibitory systems , 1996 .

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

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

[13]  K. Osen Course and termination of the primary afferents in the cochlear nuclei of the cat. An experimental anatomical study. , 1970, Archives italiennes de biologie.

[14]  B. Norris,et al.  Tonotopic organization of the anteroventral cochlear nucleus of the cat , 1981, Hearing Research.

[15]  D. Oertel,et al.  Inhibitory circuitry in the ventral cochlear nucleus is probably mediated by glycine , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  R V Shannon,et al.  Auditory Brainstem Implant: II. Postsurgical Issues and Performance , 1993, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[17]  E. Brunner,et al.  Inhibition of GABA Metabolism in Rat Brain Slices by Halothane , 1981, Anesthesiology.

[18]  F. Zeng,et al.  Speech recognition with altered spectral distribution of envelope cues. , 1996, The Journal of the Acoustical Society of America.

[19]  R. Moore,et al.  A comparative study of the superior olivary complex in the primate brain. , 1971, Folia primatologica; international journal of primatology.

[20]  W. A. Hagins,et al.  Dark current and photocurrent in retinal rods. , 1970, Biophysical journal.

[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]  K A Frey,et al.  Demonstration of prosthetic activation of central auditory pathways using [14C]‐2‐Deoxyglucose , 1990, The Laryngoscope.

[23]  R V Shannon,et al.  The Multichannel Auditory Brain Stem Implant: Performance in Twenty Patients , 1998, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[24]  E. Rouiller,et al.  The central projections of intracellularly labeled auditory nerve fibers in cats , 1984, The Journal of comparative neurology.

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

[26]  Allen F Ryan,et al.  Spatial distribution of neural activity evoked by electrical stimulation of the cochlea , 1990, Hearing Research.

[27]  W. Warr Fiber degeneration following lesions in the multipolar and globular cell areas in the ventral cochlear nucleus of the cat. , 1972, Brain research.

[28]  J. P. Mobley,et al.  Electrical stimulation of the auditory brain stem structure in deafened adults. , 1987, Journal of rehabilitation research and development.

[29]  G. C. Thompson,et al.  HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat , 1981, The Journal of comparative neurology.

[30]  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.

[31]  Y. Yaari,et al.  Halothane Blocks Synaptic Excitation of Inhibitory Interneurons , 1996, Anesthesiology.

[32]  T. Narahashi,et al.  General anesthetics modulate GABA receptor channel complex in rat dorsal root ganglion neurons , 1989, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[33]  D. McCreery,et al.  Stimulation with chronically implanted microelectrodes in the cochlear nucleus of the cat: Histologic and physiologic effects , 1992, Hearing Research.

[34]  Bruce J. Gantz,et al.  Iowa cochlear implant clinical project: Results with two single‐channel cochlear implants and one multi‐channel cochlear implant. , 1985, The Laryngoscope.

[35]  D. Eddington,et al.  Speech Recognition Experience with Multichannel Cochlear Implants , 1985, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

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

[37]  N. Strominger,et al.  The cytoarchitecture of the human anteroventral cochlear nucleus , 1973, The Journal of comparative neurology.

[38]  R V Shannon,et al.  Speech recognition as a function of the number of electrodes used in the SPEAK cochlear implant speech processor. , 1997, Journal of speech, language, and hearing research : JSLHR.

[39]  R. Shannon,et al.  Multi-unit mapping of acoustic stimuli in gerbil inferior colliculus , 1997, Hearing Research.