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Effects of Stapedius-Muscle Contractions on Masking of Tone Responses in the Auditory Nerve

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Effects of Stapedius-Muscle Contractions on Masking of Tone Responses in the Auditory Nerve Effects of Stapedius-Muscle Contractions on Masking of Tone Responses in the Auditory Nerve RLE Technical Report No. 544 May 1989 Xiao Dong Pang Research Laboratory of Electronics Massachusetts Institute of Technology Cambridge, MA 02139 USA a e a a -2- EFFECTS OF STAPEDIUS-MUSCLE CONTRACTIONS ON MASKING OF TONE RESPONSES IN THE AUDITORY NERVE by XIAO DONG PANG Submitted to the Department of Electrical Engineering and Computer Science on April 29, 1988 in partial fulfillment of the requirements for the Degree of Doctor of Science ABSTRACT The stapedius muscle in the mammalian middle ear contracts under various condi- tions, including vocalization, chewing, head and body movement, and sound stimulation. Contractions of the stapedius muscle' modify (mostly attenuate) transmission of acoustic signals through the middle ear, and this modification is a function of acoustic frequency. This thesis is aimed at a more comprehensive understanding of (1) the functional benefits of contractions of the stapedius muscle for information processing in the auditory system, and (2) the neuronal mechanisms of the functional benefits. The above goals were approached by investigating the effects of stapedius muscle contractions on the masking by low-frequency noise of the responses to high-frequency tones of cat auditory-nerve fibers. The following considerations led to the approach. (1) Most natural sounds have multiple spectral components; a general property of the audi- tory system is that the responsiveness of individual auditory-nerve fibers and the whole auditory system to one component can be reduced by the presence of another component, a phenomenon referred to as "masking". (2) It is known that low-frequency sounds mask auditory responses to high-frequency sounds much more than the reverse. (3) Noise in natural acoustic environments is predominantly of low frequency. (4) Contractions of the stapedius muscle attenuate low-frequency sounds much more than high-frequency sounds. (5) There have been human psychoacoustic studies which suggest that contrac- tions of the stapedius muscle significantly improve (A) the detection of high-frequency tones masked by low-frequency noise and (B) the identification of speech signals at high intensities (at high intensities, masking of the high-frequency components of speech by its low-frequency components becomes considerable). There were four aspects of the investigation: (1) measurement of the stapedius- induced attenuation of sound and the determination of whether the attenuation depends on sound level; (2) measurement of the masking of auditory-nerve fiber responses to 6 -3- and 8 kHz tones by continuous low-frequency narrow-band noise (300Hz bandwidth cen- tered at 500Hz); (3) measurement of the effects of stapedius contractions on the masking of auditory-nerve fiber responses; and (4) a test of a mechanistic model which attempts to explain the results of (3) from the results of (1) and (2). The measurements were made with the stapedius muscle activated by artificial electric stimulation (activation of the stapedius muscle by the central nervous system was blocked pharmacologically). Results show that (1) For a given level of stapedius contraction, the attenuation of sound does not depend on sound level. (2) The stapedius-induced attenuation of low- frequency sound reduces masking by low-frequency noise of auditory-nerve fiber responses to high-frequency tones. Unmasking effects up to 40 dB were observed; the data suggest that unmasking up to 75 dB might occur in some fibers. (3) The observed unmasking effects of the stapedius contractions on auditory-nerve fiber responses can be completely explained by the mechanistic model which predicts the unmasking based only on the growth-rate of neuronal masking and the stapedius-produced linear attenuation of sounds reaching the inner ear. (4) The average growth-rate of neuronal masking was 2 dB/dB for the maskers and signals studied. (5) Maximum growth-rate of masking and maximum stapedius-unmasking occurs in auditory-nerve fibers whose characteristic fre- quencies are near the test-signal frequency. It is concluded that (1) The determination of linearity of stapedius effects on middle-ear transmission makes it possible to (A) predict stapedius effects on auditory responses in general and (B) simulate stapedius filtering at any stage before the cochlea. (2) The observed stapedius-unmasking in auditory-nerve fibers is adequate to explain the stapedius-unmasking reported from psychophysical experiments. (3) The quantitative model of the stapedius-unmasking is equally applicable to neuronal as well as to psychoacoustic responses, and is in particular applicable when the stapedius muscle is activated through the acoustic reflex (i.e., with "closed-loop" regulation of acoustic transmission through the middle ear). (4) Stapedius-unmasking on the order of 40 dB is achievable with physiological activation of the stapedius muscle such as with vocaliza- tion. (5) An important function of the stapedius muscle is to improve acoustic communi- cations both in noisy environments and for high-intensity acoustic signals with low and high frequency components (such as human speech). Such a function might be of impor- tant survival value. Furthermore, a simulation or augmentation of "stapedius filtering" in hearing-aid devices might provide significant help in dealing with some wide-spread hearing-impairment problems. Thesis Supervisor: Dr. John J. Guinan, Jr. Title: Principal Research Scientist in Electrical Engineering and Computer Science -4- To my parents and my wife Sw -5- Acknowledgments There are many people whom I want to thank. I thank MIT (as a collective of people) for giving me a good education in many dimen- sions. Many members of the Eaton-Peabody Laboratory, where the experimental work of this thesis was conducted, helped me in various ways. I thank you all. While it would be difficult to enumerate all of the ways they helped, some deserve special mention. Monique Bourgeois, Paul Davis, Leslie Dodds, Vijay Gandevia, and Debbie Learson performed the lengthy and demanding surgical preparations with great care, and taught me about various aspects of animal surgery and care. Monique also contributed to the histology work. Anna Graybeal participated in data process- ing. John Ledwith summarized the thesis for me by helping prepare the summary figure. I would like to express my gratitude to the engineers, Bob Brown, Mark Curby, Charlie Gage, Ishmael Stefanov-Wagner, and Dave Steffens, who provided prompt and quality technical support upon every request, and many times more assistance than I requested. They not only fixed hardware problems or came up with the software needed but also frequently went on to tell me how they did it, thus increasing the benefits I received by many dB. My special thanks go to Drs. Jim Kobler and Sylvette Vacher, who taught me the surgical approach to the stapedius muscle. I would like to thank Barbara Kiang, not only for her generous assistance with the histology work, but also for her general support and care. Dr. John Rosowski gave me introductions to both Chamber III and Americanisms (sorry I can't remember the Polish words you told me). I am thankful to Dr. Bertrand Delgutte for inspiring discussions and Dr. Charlie Liberman for instruc- tions on various aspects of electrophysiological experiments. My thanks also go to Dr. Ruth Ann Eatock for her spiritual support in the early and most difficult phase of this research by sharing with me her experience with the lizard auditory nerve when I was struggling in those long nights trying to figure out how to record from cat auditory-nerve fibers. I wish to thank my fellow gra- -6- duate students, Scott Dynes, Mike McCue, Jennifer Melcher, and Houston Warren, for good com- pany, each in his or her own way. While the exchange of 2:00 AM jokes with Houston through the computer helped to keep both my wife and me awake, his contribution in my "de-efferented" animal experiments was crucial. I was especially touched when I learned afterwards that Houston gave up his classes to help with my experiment (his medical-school classes, his dream classes). Jennifer's support always came in when I was most unsatisfied with my experiments, by per- sistently pointing out to me the "bright side". I sincerely appreciated all the warm help from Mike, from chamber wiring to MacDraw, among other things. Each member of my Thesis Committee, Drs. John Guinan, Steve Colburn, Larry Frish- kopf, Nelson Kiang, and Bill Peake, has contributed in a unique way. I am grateful to my thesis supervisor, Dr. John Guinan, for helpful criticisms, advice, assistance and support in every phase of this thesis research. I learned much from him both in technical capabilities and in the knowledge of the whole auditory system. Thanks are due to Dr. Larry Frishkopf and Dr. Steve Colburn for their encouragement and insightful suggestions in the preparation of this thesis. They broadened my view. There is, of course, Dr. Nelson Kiang, Director of the Laboratory. He has had a great influence on my training in scientific thinking, and his care for my overall well-being was felt in many ways. I am indebted to Dr. Bill Peake for showing me an example of a great teacher in every capacity. It is such a privilege to have been in close association with him, and his impact on me will remain for many years to come. My gratitude is due to the late Chairman of the General Chamber of Commerce of Hong Kong, Mr. K. C. Wong. It was his kindness and generosity that made my coming to the United States in 1981 possible. I would like to express my appreciation of the continuous support and friendship of Nat Durlach, my first supervisor at MIT, and my appreciation of the spiritual support of Dr. Francis Lee. I* )r P C r*l pi U. ·LI -7- The friendship of Helen Peake is greatly appreciated.
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