Neural Encoding of Sound Sensation Evoked by Electrical Stimulation of the Acoustic Nerve

Abstract

A series of psychoacoustic experiments was conducted in subjects implanted with a permanent intracochlear bipolar electrode. These experiments were designed to reveal the nature of the sensation evoked by direct sinusoidal electrical stimulation of the acoustic nerve. A series of single unit experiments in the inferior colliculus of cats was then conducted, using intracochlear stimulus electrodes identical to those implanted in human subjects in all respects except size, and using identical stimuli. These physiological experiments were designed to reveal how sounds evoked by intracochlear electrical stimulation in humans are generated and encoded in the auditory nervous system. Among the results were the following: 1) The sensation arises from direct electrical stimulation of the acoustic nerve. It is not “electrophonic” hearing arising from electro-mechanical excitation of hair cells. 2) While sounds are heard with electrical stimulation at frequencies from below 25 to above 10,000 Hz, the useful range of discriminative hearing is limited to frequencies below 400–600 Hz. 3) There is no “place” coding of electrical stimuli of different frequency. Tonal sensations generated by electrical stimulation must be encoded by the time order of discharge of auditory neurons. 4) The periods of sinusoidal electrical stimuli are encoded in discharges of inferior colliculus neurons at frequencies up to 400–600 Hz. 5) Both psychoacoustic and physiological evidence indicates that the low tone sensations evoked by electrical stimulation are akin to the sensations of “periodicity pitch” generated in the normal cochlea. 6) Most cochlear hair cells are lost with intracochlear implantation with this electrode. Most ganglion cells survive implantation. Implications of these experiments for further development of an acoustic prosthesis are discussed.

Hearing restoration: Graeme Clark, Ingeborg Hochmair, and Blake Wilson receive the 2013 Lasker~DeBakey Clinical Medical Research Award

“…At UCSF, a team that included otologist Robin Michelson and neurophysiologist Michael Merzenich, among others, implanted a group of patients with a single electrode implant each (13). The results from these patients were similar to those reported by House.…”

The Early History of the Cochlear Implant

“…The team at the University of California, San Francisco (UCSF), under the supervision of otolaryngologist Robin Michelson and with the collaboration of otolaryngologist Robert Schindler and neurophysiologist Michael Merzenich, became interested in the development of a CI. Merzenich conducted various studies at the turn of 1970 on cats 35 and was interested, contrary to Michelson, in the development of a multichannel CI. After these animal experiments, the UCSF team selected 4 patients who were tested with an electrode placed temporarily in the lower scala under local anesthesia.…”

“…The reports of this first congress were published 1 year later and specially distributed to the participants. 38 By this point, the term cochlear implant had been definitively introduced into the medical literature.…”

Personal reflections on the multichannel cochlear implant and a view of the future

“…To achieve place coding, Merzenich et al first focused their research on inserting a molded electrode array in the scala tympani to fill the space [33][34], thus limiting the spread of current around it. They also showed that current was best localized with bipolar stimulation of the peripheral auditory nerve fibers in the cochlea, with current flowing in a radial rather than longitudinal direction ( Figure 5).…”