Author Institution: University of Rocheste

Culler, E. A.

The Ohio Journal of Science

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RESEARCH ON THE CENTRAL AUDITORYMECHANISMS: SOME RECENT METHODSAND RESULTS1E. A. CULLER,University of RochesterWhenever I speak upon the topic of hearing, I am reminded of anincident which occurred some years ago at a meeting of the NationalAcademy of Science. A young man from one of our large universitieshad just reported a study in audition. As he concluded, Dr. Cattellarose—dean of American psychology and Nestor of American science.His first comment was to this effect: "Whenever you think you'vediscovered something new about hearing, turn to Helmholtz and you'llfind it there." This tribute to the greatest experimental theorist in thehistory of acoustic research was indeed well deserved; but it was con-siderably more true when spoken fifteen years ago, than it is today.We now know some things about hearing that even Helmholtz, with hisunrivaled insight, did not perceive.This new knowledge is due, in large part, to new methodology. Ineed not remind you that the milestones in scientific progress aremarked by new methods of research. Emphasis upon methodology isa cardinal distinction between the man in the laboratory and the manon the street. Whenever I speak to laymen about our work, I am oftenreminded by my hearer that he is not interested in methodology; whathe wants are facts. He makes the statement with something of an air,as though he prided himself on being hard-headed and practical. Butwe all know, if we know anything about science, that the observationswe get are a function of the methods we employ; that facts are the fruitof operations. For that reason let us begin with a few methods that arebasic in auditory research as a means to understanding some of thefacts which I wish to report.The first method historically was doubtless clinical. If everybodyhad perfect and uniform hearing from birth until death, never sufferingany impairment because of accident or disease, it is doubtful thathearing would ever have been a problem. Because some of us hearbetter than others, because we hear better early in life than later,because hearing may be completely destroyed through some injury, weare forced to think about the mechanisms of hearing—how they operateand what can be done to restore them. In other words, the accidentsof Nature prod man to research. In this sense, Nature may be calledthe first experimenter. One of the great contributions of Darwiniantheory is its revelation that the world we inhabit is an experimentalinstead of a static universe. In the clinical method Nature sets theCommunication No. 37 from the Laboratory of Physiological Psychology(Animal Hearing), which was transferred from the University of Illinois to theUniversity of Rochester in 1938. This laboratory is maintained with aid fromthe Research Council, American Otological Society.117118 E. A. CULLER Vol. XLIproblem and man tries to solve it. A patient .whose hearing disturbshim appears in the consulting room of an otologist; who thereupon, inaddition to other tests, plots a complete audiogram of each ear. Hethus determines as well as possible the locus and nature of the malady.Ofttimes little can be done beyond prescribing a hearing-aid. Thepatient is then examined year by year to note what changes occur andfinally, if the physician lives long enough and the patient dies soonenough, the ears which have been so often tested are removed andsectioned in order to correlate their anatomical deficiency with thefunctional hearing-loss. The procedure is sound but has several greatdefects. 1. It is insufferably slow. The patient may live longer thanthe physician; so that the answer to a simple question of fact may requireseveral generations of careful work by many investigators. 2. But astill graver difficulty is that Nature, although the first experimenter, isunquestionably one of the poorest. A young man of the laboratory,who could not plan his experiment better than Nature does, wouldfind it hard to win even a bachelor's degree. A clinical lesion usuallyimplicates so many separable factors in the ear that it is quite impos-sible to say which one is responSilbe for the hearing-loss. At JohnsHopkins Medical School is located one of the world's most extensivecollections of sectioned human ears, together with audiograms showingthe functional condition of each one. This vast body of material hasaccumulated over many decades and represents a huge expenditure oftime, energy, and money; yet I venture to say that we can learn moreby the use of modern experimental techniques in six months from acageful of guinea pigs about localization of function in the cochlea thanwe can from this great assemblage of clinical evidence. While theclinical method will never be superseded, its deficiencies are such thatlittle real progress could be made until adequate experimental methodswere devised.Of these experimental methods, the first to consider is conditioning.This term is familiar to you. It was bestowed by the Russian physiol-ogist Pavlov and is illustrated in one form by the familiar laboratorypicture in which a dog stands with one foot resting upon a metal gridwhich can be charged with a small electric potential. If you sound atone about two seconds before the paw is stimulated, the animal willsoon begin replying to the tone by withdrawing his foot from the grid.We say that he has been "conditioned" and now reacts to the soundas he formerly did to the shock. After conditioning has been estab-lished, the tone is made weaker and weaker. The animal continues toreact as before until at last he begins to falter, responding sometimesbut not always. With continued reduction of intensity, a point is even-tually reached where no response occurs at all: this implies that the toneis now completely inaudible. This simple procedure has proved extraor-dinarily fruitful in studying problems of hearing. The older exper-imenters, who tried to get away from the limitations of the clinic, wereimpaled upon one horn of a dilemma. If they worked with humanpatients, they could test the subjects's hearing but they could notoperate surgically on him. After all, we can't drill a hole in our neigh-bor's ear to see how that would affect his hearing. If, however, theyNo. 3 CENTRAL AUDITORY MECHANISMS 119tried to use animals, they could indeed operate on the subject but theywere unable to measure what it could and could not hear. Until veryrecent times, effective laboratory research on hearing was blocked bythis dilemma. Now, however, by the conditioning procedure we cantrain a dog or cat or guinea pig to react visibly to every sound it canhear, however faint, and thereupon measure its audiogram. We canthen anesthetize the animal and make some well defined lesion in theacoustic tracts. As soon as the animal recovers from anesthesia, it willtell us by its reactions the exact effect of our lesion. By making com-parative tests on our trained animals and on ourselves, we have provedthat a test-animal is fully as reliable a witness as a good human patient.Almost every problem that arises in the otological clinic with humanbeings can now be tested with experimental controls in the animallaboratory.Another experimental method which has proved of the greatestvalue in recent years is electrical. It has long been known that theactivity of living cells is often attended by electric phenomena. Sowell was this understood even fifty years ago that these electric poten-tials were designated "signs of life." One could, for example, distinguisha living seed from a dead one by means of the minute electric currentsgenerated by the former. There are, of course, other signs of life. Aliving cell will give off CO2 at all times; an active cell will emit more CO2than a cell which is resting. This has been well demonstrated by aninstrument known as the biometer or "life meter," which reveals thatan active nerve fiber gives off fully twice as much carbon dioxide asthe same fiber when at rest. Likewise living cells when active emitheat; even the minute nerve-cells generate small quantities of heatwhen they are conducting impulses. The peculiar advantage of electricalprocedure is, however, that living cells can be studied in situ morereadily than by any other means. Electric techniques are so highlydeveloped that we can put an electrode against the inner ear or theauditory nerve, pick up the minute potentials therein generated, leadthem through an amplifier into an oscillograph, and study their prop-erties. The contribution of this method to understanding the functionof the ear and its associated tracts is hard to overstate. What we maycall the modern period of auditory investigation begins with the appli-cation of electric methods to the study of the cochlea and the cochlearnerve.In many cases the two experimental methods, electric and con-ditioning, are applicable to the same problem. When used in combina-tion, they constitute an extremely powerful tool for the study of acousticmechanisms.In recent years research by use of these methods has been principallyof two kinds. 1. Some investigators have continued to study the activityof the cochlea in different animal-forms and to seek an adequate descrip-tion of the peripheral structures and operations by which a sound-waveis converted into discrete nerve-impulses. 2. Others have examinedthe structural characteristics and functional problems of the neuralconduction-system in its course from cochlea to cortex; the purpose ofthese studies being to describe and evaluate the neural events whichunite the functional levels of the acoustic system.120 E. A. CULLER Vol. XLIIt may be well to remind you that both the cochlea of the inner earand the neural components of the acoustic system emit electric poten-tials when sound vibrations are impressed upon the ear. These twotypes of potential, however, differ in certain important respects. 1.Synchronized cochlear potentials can be detected as high as 6000 cyclesor more whereas synchronized neural potentials seldom are reportedbeyond 2500 or 3000 cycles. 2. The cochlear potential usually resembles(apart from aural distortion) the wave form of the impressed sound,whereas the neural potentials look like similar potentials in othersensory nerves, being essentially monophasic and negative. 3. Thecochlear voltages are many times as large as the neural, with the resultthat they spread by ordinary electric transmission to points severalcentimeters away from their origin. The neural potentials being muchfeebler can usually be detected only in close proximity to the nerve-cellwhich generates them. 4. Cochlear electrophonics, which thus spread inall directions by ordinary transmission, travel at considerably highervelocity than do neural impulses which propagate at the usual speed ofnerve-impulses (e. g., 30 meters per second). 5. Cochlear potentialseffectively resist narcosis whereas neural potentials are appreciablyreduced by most anesthetics. 6. Cochlear potentials may persist forminutes or even hours after demise of the animal, though with reducedintensity, whereas the neural potentials commonly disappear at or justprior to death.In accord with the original plan of this symposium, I shall confinemyself principally to reporting some studies bearing upon the phenomenathat occur in the neural acoustic system central to the cochlea; that is,studies which belong to the second group of investigations justmentioned.1. I shall first notice a study now in progress by W. D. Neff of ourlaboratory on the effects upon hearing in the cat of partial section of theeighth nerve. Changes in sensitivity occasioned by local damage tothe eighth nerve, which connects the cochlea to the brain stem, areobserved by the conditioned-response technique. The cat is first con-ditioned until it responds clearly to any audible sound. The audiogramof the animal is then measured at the various octave frequencies from125 cycles to 8000 cycles and, in some cases, for two additional octaves(62 cycles and 15000 cycles). When the animal's normal hearing is thusdetermined, the cochlea of one ear is destroyed so that all auditoryimpulses must pass to the brain via the nerve that is later to be partiallysectioned. Destruction of the single cochlea results in surprisingly smallloss of total sensitivity, usually about two or three decibels. (A decibelis the standard unit in acoustic measurements and is, very roughly,that difference in physical intensity of two tones which can just beperceived by a normal ear). As soon as the animal's thresholds for theseveral frequencies have been determined for the one remaining ear,the second and critical operation ensues. Under complete narcosis theeighth nerve of the intact ear is carefully exposed. The nerve tissuebeing quite soft can be removed in any desired amount by a suction-pipette so that part of the nerve is left intact but the remaining fibersare effectively interrupted. After the animal is sufficiently recoveredNo. 3 CENTRAL AUDITORY MECHANISMS 121for testing, the postoperative limens are secured. Comparison of theselimens with those which preceded the operation will, obviously, revealthe losses due to partial section of the nerve. Results to date revealthat a very small lesion brings no significant loss at any frequency,whereas with larger lesions, marked losses appear at several of thehigher frequencies. Since the experiment is not yet complete and his-tological evidence is not yet available, interpretation must be tentative;but several conclusions are already obvious. First, not all fibers of theeighth nerve need be severed to render an animal deaf to certain fre-quencies. Secondly, the remaining intact fibers give at other frequenciesthe same sensitivity (limen) as did the whole nerve.2. A second study was performed by Ades and his collaborators atthe level of the medial geniculate bodies in the cat. These two nuclei,right and left, being the final way-station from cochlea to cortex, providean ideal site for determining in what manner cochlear impulses aretransmitted to the brain. The general procedure was as follows: Theintact cat is first conditioned and its normal audiogram obtained for anadequate sample of the audible range (octave frequencies from 125 to8000 cycles). Localized electrolytic lesions are then effected at cor-responding points of the two medial geniculates. The cat is then retestedto determine what losses, if any, have occurred in its hearing. Finally,the animal is dispatched and the brain prepared and examined byhistologic methods.Inspection of the audiograms shows that localized lesions in sym-metrical areas of the two geniculates result in some attenuation of audi-tory sensitivity for all frequencies tested, but that the degree ofimpairment differs widely. The variation is not haphazard but in everycase conforms to a definite pattern, the loss being greatest at one or twofrequencies, graduating down to a minimum at those most distantfrom the focal frequencies. Cats with lesions in corresponding areasdisplay a similar distribution of hearing losses. Loci for the severalfrequencies seem to be as follows: 8000 cycles, dorsal region; 4000,anterior; 2000, lateral; 1000, posterior; 500, medial. The lower fre-quencies, 250 and 125 cycles, were in no case attenuated to maximaldegree, but apparently traverse the ventral side. The several loci thusappear to follow a linear course, beginning with higher frequencies inthe dorsal section and circling downward to the ventral region wherethe lower frequencies appear.3. The medial geniculate nucleus in the cat has also been explored byCoakley, using an entirely different method. If there is a spatial distri-bution of fibers within the nucleus, it should be possible to determinetheir position by recording the electric potentials generated in anygiven case by the active units. Accordingly, the distribution of poten-tials in the nucleus has been studied for five frequencies of stimulationarranged in octave steps from 125 to 2000 cycles. Since the potentialsabove 3000 cycles became so feeble as to be practically imperceptible,our data are limited to frequencies below that point. The potentialsgenerated by an impressed tone were measured at about 120 pointsarranged uniformly throughout the nucleus and just beyond its margins.Of course only a small number of points could be studied in any one122 E. A. CULLER Vol. XLIanimal but each point was examined in about six cats. Summarizing theresults for all animals, we find that for each frequency applied to the ear,the potentials are maximal for amplitude in one region and becomesmaller as the needle is moved in any direction from this area. If thesemaxima are arranged in order of frequency, they constitute a figure sim-ilar to a conical helix. Further analysis of the data reveals the approx-imate course followed by each group of fibers. In addition exactsynchronization between impressed frequency and neural pulses in thenucleus was observed up to 2500 cycles. This implies that, whatevernumber of negative (or positive) pulses is generated in the cochlea, thesame number will still be found (up to 2500 cycles) in the neuralaction-currents of the medial geniculate.4. E. A. Lipman has accumulated some material on cortical functionin hearing-. The procedure is similar to some already mentioned. Thenormal audiogram of a trained dog is first measured at the usual repre-sentative frequencies (125 to 8000 cycles). The entire temporal(acoustic) area of one side of the cortex is then removed and the animal'saudiogram again tested. Even though only one side of the brain is nowintact, hearing-losses are quite negligible, being in no case more thanthree or four decibels. The second and critical operation then followsin which a small localized part of the remaining intact side is removedwith the suction-pipette. Postoperative tests again reveal what losses,if any, occur at each frequency.In general the losses at a specific frequency are not large, about 10decibels, but the results to date indicate that hearing losses are con-fined to the area comprised by the medial and posterior ectosylviangyrus and the adjacent medial and posterior sylvian gyrus. Removal ofcortex beyond this area seems to have no effect upon hearing. Thus farlesions in the ectosylvian gyrus are followed by losses at 500 cycles andbelow, whereas lesions in the adjacent sylvian area seem to bring lossesat higher frequencies from 1000 cycles up. These results indicate thatfocalization of responses is not so sharp as elsewhere but still present.The exact locus for each of the several frequencies awaits further tests.From these and other observations we may infer that different tonalfrequencies, when impressed on the ear, actuate different areas orpatterns of receptive cells within the cochlea and that the impulses thusgenerated traverse differential pathways to the auditory projectioncenter of the cortex; but that the number of pulses per second passingto the cortex rises in step with the impressed tone, and thus provides asecond clue by which the organism can perceive pitch. The relativecontribution of these two factors (spatial and temporal) must awaitfurther analysis.

Research on the Central Auditory Mechanisms : Some Recent Methods and Results

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Research on the Central Auditory Mechanisms : Some Recent Methods and Results

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