the opossum ear and evolution of the coiled cochlea

The Opossum Ear and Evolution of the Coiled Cochlea

CBSAR FERNANDEZ AND ROBERT S . SCHMIDT 1 Department of Surgery, The University of Chicago, Chicago, Illinois

A comparison of the cochlear physiology and anatomy of the opossum, a marsupial, with contemporary placental mammals provides an opportunity for studying the evolution of the mammalian cochlea.

The data from Larsell, McCrady and Zimmermann ('35), McCrady, Wever and Bray ('37 and '40), McCrady ('38), Lar- sell, McCrady and Larsell ('44) revealed that differentiation of the organ of Corti starts in the upper basal and adjacent lower medial coils in the 48 day old opossum. With further development the differentiation on the cochlea's cytoarchitecture extends simultaneously toward both apex and base. This progressive development is associated with changes in cochlear responses as measured by the cochlear microphonics. Microphonics were recorded on the forty-eighth day, (the earliest stage tested), in response to sound stimuli ranging from 1,000 to 7,000 cps. The frequency range expands rapidly in both directions during the next ten days. In the final developmental stage (about 75 days after birth) cochlear microphonic responses to sound stimuli between 200 and 20,000 cps were recorded.

These investigations showed that both the anatomy and physiology of the opossum's cochlea exhibit considerable similarities to the anatomy and physiology of placental mammals. It would be of general interest for the theories regarding evolution and development of the cochlea to supplement the previous observations with a comparative study of other cochlear potentials described in placental species (guinea pig, cat, monkey). These animals present a complex electrical phe- nomenon of the cochlea which is formed by several classes of potentials.

First of all, the endolymph of the cochlear duct, including the tectorial membrane, is about 80 mV positive with respect to the perilymph or the neck muscles.

This DC potential, originally described by von Bkkksy ('52a) and also called the endocochlear potential by Davis ('57), is sensitive to oxygen deprivation. Under anoxic conditions in drops from positive to negative values (von BCkCsy, '52b; Gis- selsson, '55; Konishi, Butler and Ferntin- dez, '6 1 ) .

Other potentials are those representing the response of the cochlea to stimulation by sound, that is, cochlear microphonics, summating potentials and action potentials. The properties of the neural components, either recorded from single units (Tasaki, '54), or as compound action potentials, are like those of other medul- lated nerves. The cochlear microphonics and summating potential are considered as receptor potentials (Davis, '61). For further details regarding the electrical phe- nomena of the cochlea see the compre- hensive work of Davis ('57).

The present investigation was under- taken with the purpose of comparing the anatomy and physiology of the adult opossum's cochlea with the anatomy and physiology of the cochlea of placental mammals. The results may help in the understanding of the evolution of the hearing sense organ in mammals.

METHODS

The experiments were carried out on six adult opossums (Didelphis viriginiana, from Florida), anesthetized with pento- barbital sodium (Nembutal). Usually an initial dose of 4.0 cm3 of Nembutal was given intraperitoneally and additional doses of 1.0 cms each were injected when necessary to maintain the animal under deep anesthesia. In all cases tracheoto- mies were performed.

1 Aided by Research Grant: B-682 ( C , ) . BT-469 (Cz) and NB-K3-17,856 from Natlonal Instltutes of Health, U.S.P.H.S.

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152 CESAR FERNANDEZ AND ROBERT s. SCHMIDT

The surgical procedure for exposing the middle ear cavity and round window niche was done as described by McCrady, Wever and Bray (’37). The approach requires a gentle handling of tissue as damage to the ossicular chain, and hence a drop in cochlear responses, can be easily produced.

Tone - bursts of frequencies ranging from 100 to 10,000 cps were used as sound stimuli. This restriction on the frequency range is due to limitations in our generating and reproducing system of tone-bursts. The duration of the tone- burst was of eight or more milliseconds and the rise-fall time was about one milli- second. The sound stimuli were delivered through a plastic tube attached to the external ear of the animal.

The cochlear responses to sound stimuli were recorded with an enameled silver wire electrode (100 11 diam.) whose tip was flattened and the enamel removed. The electrode was mounted on a micromanipulator and the tip placed on the round window membrane. The ground electrode was a large silver wire embedded in cotton wet with Ringer’s solution, which was placed on the neck muscles. The responses to sound stimuli were prop- erly amplified and displayed on a dual beam oscilloscope. It was necessary to keep the round window niche and middle ear cavity free of fluid as their accumula- tion produced a decrease in magnitude of cochlear responses. Perhaps the fluid ac- cumulated in the round window provides a conductive path that effectively short- circuits the responses to sound stimuli.

For recording DC resting potentials in the cochlea. the animals were immobilized with Tubocurarine chloride ( 3 mg per cm’) and rnaintaincd under artificial respira- tion. It appears that the opossum, unlike the cat or guinea pig, requires large doses of curare to be effectively immobilized. The initial dose usually 5.0 cm5 was injected intramuscularly and in some instances it was necessary to repeat the dose in order to produce a satisfactory immobilization. After this, the basilar membrane was exposed by removing the round window niche membrane and part of the bony wall of the promontorium. A pipette (2-7 ~1 in diameter at the tip), filled with Ringer’s solution and mounted

on a micromanipulator was directed, under a dissecting microscope, through the basilar membrane into the organ of Corti and scala media. The pipette contained a silver-silver chloride electrode which was connected to a Keithley electrometer by which the DC potentials were measured directly. In some instances these potentials were recorded with a n Offner Dynograph coupled to the Keithley electrometer. The ground electrode, consist- ing of a large silver-silver chloride wire electrode embedded in cotton wet with Ringer’s, was placed on the neck muscles.

Some animals were exposed to oxygen deprivation by clamping the tracheotomy tube for four or more minutes. The behavior of the DC resting potentials in scala media was observed during and after clamping the tracheotomy tube.

After completion of the experiments the animals were sacrificed and fixed by in- travital perfusion with Heidenhain-Susa’s solution. The temporal bones were removed and treated for histological studies.

RESULTS

The recording of cochlear potentials, either from the round window or from inside the opossum’s cochlea, certainly presented more technical difficulties than did similar recordings on the cat or guinea pig. Placing the electrode on the round window membrane or introducing a micropipette into scala media is impeded by several factors such as: a narrow round window niche, fluid continually running from the operating field, and difficulty in keeping the opossum immoblized. These and other factors in the technique were considered as causing certain variability in responses among the animals of our series. And, perhaps, these factors may explain some differences between our data and that from other laboratories.

DC resting potentials. A micropipette advancing from the round window niche to scala media registered electrical events of great similarity to those described for placental mammals. When the micropipette was i n the round window niche or scala tympani, no potential difference was detected between these areas and the reference electrode on the neck muscles. As the pipette penetrated the basilar mem-

EVOLUTION OF THE COILED COCHLEA 153

brane, a negative DC potential of about 35 mV was recorded. With further ad- vance of the micropipette, a sudden change of the DC potential from -35 to as much as +98 mV took place. We assume that the reversal of the DC potential from negative to positive values occurred when the micropipette penetrated the re- ticular membrane overlying the organ of Corti. The endocochlear potential dropped to zero upon withdrawal of the micropipette. The negative DC potential of the organ of Corti was never observed during the withdrawal; in our experience this is also true with placental mammals (guinea pig, cat, dog and monkey). Repenetration through the same pathway can be associated in the opossum, and in placental mammals as well, with a considerable local fall of the endocochlear potential. The fall is local because a new penetration at one or more millimeters distance from the first puncture yields normal values of both the negative DC of the organ of Corti and the endocochlear potential. The fall occurring with re-penetrations is probably due to local damage by the micropipette. This explains the low value of the endocochlear potential in opossum E-234 illustrated in figure 1. The voltage obtained in the first penetration was +75 mV but with several punctures this was reduced to $58 mV.

The effect of oxygen deprivation on the endocochlear potential (fig. 1) was similar to that observed in placental species (Bkkksy, '52 b; Gisselsson, '55; Konishi, Butler and Fernhdez, '61). After the trachea was clamped, the endocochlear potential fell rapidly and, passing through zero, reached negative values of about -20 mV. If air was readmitted before the death of the animal then the potential recovered its original value,

Cochlear microphonics. The cochlear microphonic potential recorded from the round window reproduced both the pattern and frequency of sound stimuli (fig. 2 ) . The sensitivity of the cochlea increased from low to high frequencies. Thresholds, as determined by our procedure and instrumentation, were certainly higher than those of the guinea pig, cat or monkey.

l 0 O j

1 40

0 2 4 6 8

Fig. 1 Effect of asphyxia on the endocochlear potential of the opossum and monkey. The figure demonstrates that the behavior of the potential in the opossum followed the same pattern as it did in the monkey. In opossum E-254 (dots on the graph) asphyxia was main- tained until the death of the animal.

T i m e i n m i n u t e s

The frequency response ranged from 250 to 10,000 cps. No responses to frequencies below 250 cps were recorded in these animals and, because of limitations in our sound generating system, no at- tempt was made to observe frequencies above 10,000 cps.

The input-output functions of cochlear microphonics for frequencies ranging from 250 to 9,400 cps for one animal are presented in figure 3. The figures demonstrate clearly that the cochlear microphonic potential was a linear function of sound intensity until the point of non- linearity. After this point the curves tended to level off, reach a maximum, and then decrease. The maximum output of the microphonic response was of the order of 500 1iV for frequencies between 2,000 and 4,000 cps. Under similar ex-


Fig. 2 The cochlear microphonic response as a function of frequency in opossum E-255. The records in the left hand column correspond to tone bursts of indicated frequency. The num- bers down the center of the figure represent intensity of the corresponding tone bursts in decibels (re: 0.0002 dynes per sq. cm). These stimuli were given at intensities producing maximum output of cochlear microphonics (CM) for each frequency. The record corresponding to a 250 cps tone burst and its cochlear microphonic response were taken at a faster sweep.

perimental conditions, placental mammals such as the cat and monkey yielded responses of 1.52.0 mV for frequencies between 500 and 4,000 cps (Fern5ndez et al. '62). It is probable that further improvement in surgical and recording techniques may demonstrate larger maximum output of the cochlear microphonics. The same reasoning may apply to the summating potential and neural components. If this is true, then the main difference between the cochlear function of the opossum and that of some placental mammals would disappear.

Summating potential. In the opossum the behavior of the summating potential was essentially similar to that described in the guinea pig (Davis, Fernsndez and NIcAuliffe, '50; Goldstein, '54). The po-

tential appeared as a shift of the baseline on which the cochlear microphonics were superimposed. The observations were made by recording the responses to high frequency tone bursts from the round window. The threshold was high and the potential exhibited no latency relative to the beginning of the cochlear microphonics. Although the voltage of the summating potential increased proportionately with the intensity of the sound stimulus, its maximum amplitude was small compared to that of placental mammals (fig. 4).

Action potentials. The neural components recorded from the round window are presented in figure 4. The record shows the classical pattern of N1 and N P as described in the guinea pig (Davis, Tasaki and Goldstein, '52). The amplitude of N, increased with increasing intensity of sound stimuli, but unlike the cochlear microphonics, no point of maximum amplitude was ever reached. The largest voltage of N1 obtained in our series was 220 pV for a 4,000 cps tone burst.

The middle ear of the opossum differs considerably from that of placental species (McCrady, Wever and Bray, '37). In the opossum the lat- eral and inferior walls of the middle ear cavity are formed mainly by soft tissue; consequently there is no bulla as described in the cat or guinea pig. As pointed out by McCrady, Wever and Bray ( ' 37 ) , this primitive arrangement is probably due to the fact that in the opossum, unlike placental species, the squamosal, tympanic and petrosal bones do not fuse into a single temporal bone. The tympanic membrane and ossicles of the opossum present no fundamental differences from those of the guinea pig or cat; however, differences in shape and dimension of the ossicular chain exist between these species.

The cochlea of the opossum, as in the guinea pig, is projected into the middle ear cavity. The cochlea is formed of two and one-half coils (McCrady, '38). Two specimens were dissected for direct meas- urements of the length of the basilar membrane. The length was determined under microscopic control by adapting a hair to the plane of the basilar membrane. It was found to be 15 mm.

Anatomical studies.

EVOLUTION O F T H E COILED COCHLEA 155

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Fig. 3 Input-output functions of the cochlear microphonic response (CM) for several frequencies in Opossum E-255. The curves followed a pattern like that described for placental mammals. The maximum output of cochlear microphonics in this and the other animals never exceeded 600 pV. The sound pressure level (SPL) is given in decibels (re: 0.0002 dynes per sq. cm).

The observations with light microscopy demonstrated that both marsupials and placental mammals exhibit the same type and distribution of cells in the organ of Corti. Yet, the shape and dimensions of the cells and structures model a receptor which is almost characteristic for each species (fig. 5 ) . One prominent feature of the opossum’s cochlea is the large size

of the external sulcus cells and spiral prominence. The enlargement of the lat- ter shapes the stria vascularis in a curve similar to that found in primitive pri- mates, such as the squirrel monkey. As in placental species, no evidence of a lagena is found in the opossum’s cochlea.

The cytoarchitecture of the opossum’s ganglion of Corti, including the intragan-


Fig. 4 Cochlear responses to an 8,000 cps toile burst at 110 db SPL (re: 0.0002 dynes per sq. cm) recorded from the round wlndow of the opossum. Stim., 8,000 cps tone burst. CM, cochlear microphonic response after filtering of the summating potential and neural components. AP, neural components after filtering out of the cochlear microphonics. The summating potential is just visible as an upward deflection of the base line in the AP record. Marker, 100 p V .

glionic spiral bundle, was found to be similar to that of placental species. The size of cell bodies throughout the ganglion is about 18-20 p,

In general, no fundamental differences were found in the structures of the ves- tibular receptor of the opossum as compared to the structures of the cat and guinea pig.

DISCUSSION

Comparison of opossz~rn with placental mammals. The comparative anatomy demonstrates that there is a remarkable similarity among therian mammals (marsupials and placentals) regarding the cytoarchitecture of the cochlea. The shape and dimensions of the structures may vary, however, from one species to another (fig. 5).

Functionally, the opossum exhibits the same classes of cochlear potentials as the guinea pig and cat, but significant differences in sensitivity, frequency range and maximum amplitude of the responses to sound stimuli may be found between these animals. Quantitative differences are not restricted to these species but are found throughout the scale of therian mammals (Wever, '59, Wever, Vernon and Lawrence, '58).

183

Since the opossum'! 1 detect high frequency signals i t is reasonable to assume that the sense organ operates as a mechanical frequency analyzer like that of the guinea pig and cat. As pointed out by Davis ('61) "the mechanical frequency analyzer of the cochlea was a biological break-through.'' This mechanism, which is increasingly elaborated during the evolution of hearing, permits detection of frequencies above 4,000 cps, and perhaps frequencies above 2,000 cps. On the other hand, the volley principle operates for detection of frequencies below 2,000 cps. This seems to be a n important mechanism underlying hearing in some cold- blooded animals (Prosser and Brown, '6 1 ; Adrian, Craik, and Sturdy, '38).

The phylogenetic origin of the mechanical frequency analyzer is unknown, but with the data available we can speculate that the system was already present or adapted by the common ancestor of the marsupial and placental mammals. A thorough investigation of cochlear potentials in monotremes may provide a basis for speculation about the principles underlying hearing in therapsid reptiles from which mammals (monotremes, marsupials and placentals) evolved.

The data on the negative resting potential in the organ of Corti and that on the endocochlear potential also revealed similarities between opossum and placental species (von BBkBsy, '52 a; Tasalu and Spyropoulus, '59; Konishi, Butler and Fer- nBndez, '6 1 ) . The evidence indicates clearly that therian mammals form one group with a large anoxia sensitive endocochlear potential of 75-100 mV. The endocochlear potential of all other groups studied does not exceed 20 mV. In birds this small potential is anoxia sensitive; in cold-blooded groups it is anoxia insen- sitive (Schmidt and Fernhdez , '62). So far, no species has yet been found that fills the gap between these two DC levels. The type of endocochlear potential in monotremes may be of interest since the cochlea of this group exhibits character- istics of both birds (and crocodilians) and therian mammals (Pritchard, 1881; Kap- pers, Huber and Crosby, '60).

Origin of cd lcd cochlea. Although there may well be differences in detail, it

EVOLUTION O F THE COILED COCHLEA 157

Fig. 5 Cytoarchitecture of the cochlear receptor in four species. Notice that all present the same types of cells but shape and dimensions of structures vary from one species to another. Hem- atoxylin-eosin stain. All photomicrographs taken in the same magnification.

thus appears that the inner ear of the opossum is essentially the same as that of placental mammals. This is true of its gross anatomy, histology, and physiology (endocochlear potential, summating potential, action potential, cochlear microphonics, and frequency localization). Those differences that have been found are smaller than such differences between various species of placentals. Paleonto- logical and comparative data permit one to estimate the period during which the coiled cochlea of the therian mammals

originated. By “coiled we refer to a cochlea with more than one complete turn.

Opossums (Didelphidae) are the most primitive of the contemporary marsupials. These animals are ‘living fossils” and have changed little since Cretaceous times. The primitive nature of the opossum and the numerous close similarities of its inner ear to that of placental mammals make it improbable that the coiled cochlea of these two groups evolved independently. Rather, this type of cochlea must have been present in the common ancestor of


marsupial and placental mammals. It seems that the line leading to these two groups diverged at least by early Creta- ceous times (Colbert, '55; Olson, '44; Simpson, '59). A coiled cochlea probably evolved sometime before this. Present evidence thus suggests late Jurassic (about 140 million years ago) as the latest time for the first appearance of a coiled cochlea.

Although the exact dimensions of the cochlea in the therapsids are not known, it is clear that these mammal-like reptiles did not have a coiled cochlea (Olson, '38, '44). The various groups of therapsids for which such data is available must have diverged by middle Permian, about 215 million years ago (Olson, '59). There- fore, a coiled cochlea could not have originated before this.

The monotreme inner ear provides additional evidence as to the earliest limit of the appearance of coiling. Although there is a tendency toward coiling, not even one complete turn is formed (Pritchard, 1881; Kappers, Huber and Crosby, '60). In fact, the monotreme cochlea shows, in external iorm, a marked resemblance to the cochleas of birds and crocodilians. At the end of the monotreme cochlea there still remains a lagena.

For three reasons it seems that the immediate common ancestor of the monotremes and therian mammals lacked a coiled cochlea and that coiling thus evolved after the divergence of these groups. First, in spite of the great variety in mammalian habits and habitats, we know of no therian mammal possessing an uncoiled cochlea (Gray, '55). There is, therefore, no reason to suppose that the lack of coiling in monotremes is the result of regression. Second, a lagena is absent only in the therian mammals. This has probably been lost as a result of coiling. If a coiled cochlea, without a lagena, had evolved before the monotreme-therian divergence, it is improbable that a typical lagena could have re-evolved in the monotremes. Third, as noted above, there is no evidence that any degree of coiling occurred in, at least, the earlier therapsids. It is now generally agreed that a number of types of mammals have evolved con- vergently from the therapsid reptiles (01- son, '59; Simpson, '59). Only two of these

mammalian lines have survived - one leading to contemporary monotremes and the other to contemporary therian mammals.

Unfortunately the history of the monotremes is very poorly represented in the fossil record. It is probable. however, that the line leading to the monotreme and therian mammals diverged sometime during early Jurassic or late Triassic times (Colbert, '55; Simpson, '59) or perhaps as early as the lower Triassic (Olson, '59). Coiling (more than one turn) must have evolved in therian mammals sometime after this divergence. Therefore, the late Triassic (about 170 million years ago) seems to be the earliest probable time in which a coiled cochlea could have evolved.

Therefore, the coiled cochlea as found in contemporary therian mammals appar- ently evolved sometime between late Tri- assic and late Jurassic (between about 170 million and 140 million years ago). Further advances in the fields of paleon- tology and comparative anatomy and physiology may eventually permit a more precise estimate of the period during which coiling first appeared.

SUMMARY

The anatomy and physiology of the opossum's cochlea was compared with the anatomy and physiology of placental mammals (guinea pig, cat and monkey).

Anatomically. no fundamental difference in the cytoarchitecture of the inner ear was found between these therian mammals. Yet, shape and size of structures may vary from one species to another.

Functionally, all these mammals exhibited the same cochlear potentials in response to sound stimuli and the same DC resting potentials within the cochlea. Dif- ferences between the species may be found in details such as sensitivity, frequency range and input-output relationships. The behavior of cochlear potentials during and after a period of oxygen deprivation in the marsupial (opossum) was similar to that of placental species.

These observations plus paleontological and comparative data permit one to speculate about the period during which the coiled cochlea of the therian mammals originated.

EVOLUTION OF THE COILED COCHLEA 159

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the opossum ear and evolution of the coiled cochlea

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