A Reexamination of "The Effects Of Partial Section of the Auditory Nerve"

A REEXAMINATION OF "THE EFFECTS OF PARTIAL SECTION OF THE AUDITORY NERVE" [1] NELSON Y. S. KIANG* Every so often in scientific work a body of facts becomes interpretable in terms of a central dogma except for a few striking observations thai are difficult to absorb. This situation demands that the experimental results be reviewed and either the observation discarded or the dogma modified. Such an example exists in auditory theory, where a study made long ago is still difficult to incorporate into a theory that regards behavioral detection of tones at threshold (at least by normal animals) as being determined by the sensitivity of individual neurons tuned to a narrow range of frequencies. I refer to the results of Dr. W. D. Neff's doctoral research at the University of Rochester done under the supervision of Dr. Elmer Culler in the late 1930s. A preliminary report of this work had been made to the Eastern Psychological Association in 1939, but a full description of the results had to await Neff's return from war-related duties [2, 3]. By then the histological data were available from Dr. Glenn Wever and others, so the combined behavioral and anatomical data were published in the 1947 volume of thefournal ofComparative and Physiological Psychology [1 , 4]. At that time there was great interest in theories ofhearing, and one of the major issues concerned how low-frequency tones were coded in the auditory nervous system, so Neff's thesis work—which presented serious problems for a strict place theory—was widely discussed. In the 4 decades since those early experiments, considerable information has been obtained on the anatomy and physiology of the auditory nerve. Yet Neff's experiments have never been repeated, and the questions raised by them have never been satisfactorily answered. It is my I wish to thank several members of the Eaton-Peabody Laboratory, K. E. Michel and E. M. Marr, for assisting in the preparation of this paper, and M. C. Liberman for the tuning curves from chamber-raised cats. This work has been supported in part by USPHS grant 5 POI NS 13126 and is based on a talk given at a symposium at the University of Chicago, May 7, 1979, to honor ProfessorWilliam Duwayne Neffin celebration ofhis sixtyfifth year. ?Director, Eaton-Peabody Laboratory of Auditory Physiology; Massachusetts Institute of Technology, Harvard Medical School, Massachusetts General Hospital, and Massachusetts Eye and Ear Infirmary, 243 Charles Street, Boston, Massachusetts 02114.© 1981 by The University of Chicago. 0031-5982/81/2402-0230$01.00 254 I Nelson Y. S. Kiang ¦ Partial Section ofAuditory Nerve intention here to review these two papers in an attempt to resolve some of these issues. The introduction to the first paper gives Neff's general perspective, which is still appropriate today: Current theories concerning the physiological processes of hearing are based largely upon evidence from studies of cochlear function and studies of the anatomical projection of the cochlea upon auditory centers in the central nervous system. Facts so derived may indicate that the auditory system can work in a given manner, but they cannot establish that the system does work in that manner . To obtain further refinement of our theories we need more direct evidence regarding the function of the auditory system, especially of that part of the system central to the cochlea. An obvious first point ofattack is the eighth nerve. [1, p. 203] Neff went on to describe the work of Walter E. Dandy, a surgeon at Johns Hopkins who reported results of inadvertent partial sectioning of the auditory nerve during operations to sever the vestibular part of the eighth nerve for relief of vertigo and nausea in patients with Meniere's syndrome. Audiometrie tests on these patients revealed a restricted high-tone hearing loss in some cases and hearing losses over a wide range of frequencies in other cases, but never losses restricted to low frequencies [5]. Neff realized the significance of Dandy's results. If hearing losses at low frequencies could not be obtained except by eliminating the entire nerve, hearing at low frequencies could not be mediated solely by fibers restricted to a small region of the nerve. The recordings of...