Ptyodactylus Hasselquistii Puiseuxi Boutan* by Ernst Glen Wever and \Iarie-Claude Hep1p-Reymond

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AUDITORY SENSITIVITY IN THE FAN-TOED GECKO, PTYODACTYLUS HASSELQUISTII PUISEUXI BOUTAN* BY ERNST GLEN WEVER AND \IARIE-CLAUDE HEP1P-REYMOND

AUDITORY RESEARCH LABORATORIES, DEPARTMENT OF PSYCHOLOGY, PRINCETON UNIVERSITY Communicated January 16, 1967 This is the third in a series of reports on the hearing of gekkonid lizards as shown by the cochlear potentials."l 2 These lizards are distinctive in a number of respects. They are active in the production of vocal sounds, are of nocturnal habit, have large eyes with vertical slit pupils, and most of them possess adhesive pads on the toes whereby they are able to climb on vertical walls and the underside of rough sur- faces. Our previous studies were concerned with the auditory capabilities of Gekko gecko, Hemidactylus turcicus turcicus, and Coleonyx variegatus bogerti. Our interest in Ptyodactylus hasselquistii was stimulated by the report of Dr. Yehudah L. Werner of the Hebrew University of Jerusalem that these lizards produce cries of uncommon intensity, and their investigation has been made possible by his kind- ness in providing us with specimens collected from rocky regions of Israel. The animals have lived well under cage conditions, but have vocalized only rarely. This study is based upon observations on 15 animals. The fan-toed gecko is a small lizard, as Figure 1 shows. A representative specimen measured 12.5 cm in length over-all, and 7.0 cm from nose to vent. The external ear is a simple opening, oval in form and measuring about 2 by 0.5 mm, placed obliquely on the sides of the head. The meatus leads directly to the tympanic membrane lying about 2 mm below the surface. Procedure. -The method of recording cochlear potentials was the same as em- ployed earlier with a variety of lizard species.'-6 The animals were anesthetized by intraperitoneal injection of 20 per cent ethyl carbamate in a dosage of 0.01 ml/ gm of body weight. The round window niche was exposed through an opening in the throat region (Fig. lc), and a fine silver bead electrode was placed on the round window membrane. Tones were introduced into the ear through a tube sealed over the external auditory meatus, and sound pressures were measured by means of a probe tube whose end portion ran concentrically with the sound tube and termi- nated at the meatal entrance. Body temperature was maintained at 240C. Results.-Sensitivity was measured by presenting various tones over a range usually from 100 to 10,000 cycles per second (cps) at the sound pressure necessary to produce a response of 0.1 microvolt (rms). Results for two of the more sensitive animals are given in Figure 2, and for two others of about average sensitivity in Figure 3. As shown, the sensitivity is greatest in the region of 700-1,000 cps, and rapidly becomes less for higher and especially for lower tones. Occasionally it was possible to record responses up to 15,000 or 20,000 cps, but it was regularly observed that measurements in this high-frequency region were hazardous: sustained stimulation with tones in this region at the levels necessary to obtain readings often produced a general impairment of responsiveness. For this reason, all tests at the high frequencies were made as brief as possible, and were usually avoided in animals whose general sensitivity was found to be poor. 681 Downloaded by guest on October 1, 2021 682 PSYCHOLOGY: WEVEIR AND HEPP-IREYMOND PROC. N. A. S.

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FIG. 1.-The fan-toed gecko, Ptyo- daclylus hasseiquiistii; (a) dorsal view, (b) lateral view, and (c) ventral view with all indication of the site of the operation for exposing the round window.

(c) The functioning of the middle-ear apparatus has been studied in a preliminary way iii several species of lizards by cutting the columella and observing the changes in sensitivity. In these observations the sound was delivered to the external ear in the same manner before and after the operation, and the only mechanical difference was the interruption of the connection between the tympanic membrane and the columellar footplate in the oval window. Figure 4 shows the effects of this operation in one specimen of Ptyodactylus hasselquistii. The plot represents the loss in decibels as a result of the interruption of the columella. As will be noted,

1 2 3 4 5 6 7 89 1 2 3 4 5 6 7 891

-60 ATTTT

100 1000 10,000 Frequency FIG. 2.-Sensitivity fulletiolss for two specimens of Ptyodactyluls hasse1quxistii. Each curve shows, for a given animal, the sounld pressure required at various frequencies to produce a standard response of ().1 microvolt. The solid line represents a femlale, and the broken line a male. Zero decibels represents 1 dynle/cm2. Downloaded by guest on October 1, 2021 VOL. 57, 1967 PSYCHOLOGY: WEVER AND HEPP-REYMOND 683

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100 1000 10,000 Frqquency FIG. 3.-Sensitivity curves for two additional specimens of Ptyodactylus hasselquistii, plotted as in the preceding figure.

the effects in the lowest frequencies vary from 10 to 20 decibels (db) and then increase steadily as the frequency is raised until a maximum is reached at 45-db for a tone of 3,500 cps, after which the effects diminish somewhat. These changes are similar in magnitude to those seen earlier in Gekko gecko, but are smaller than obtained in Hemidactylus turcicus. As has been shown in mammals, this method of measuring the efficiency of the middle ear is complicated by the presence of the tympanic membrane and the pe- ripheral, severed portion of the columella, and also by the likelihood of interaction between oval and round window pathways of stimulation. Hence the method gives only a rough indication of middle-ear function.

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FIG. 4.-The effects on sensitivity of an interruption of the columella. Downloaded by guest on October 1, 2021 684 PSYCHOLOGY: WEVER AND HEPP-REYMOND Pitoc. N. A. S.

In some of the animals, intensity functions were obtained by presenting a given tone at various levels of intensity and measuring the resulting potentials. Such a function is given in Figure 5. Here the applied intensities of a 1,000-cps tone are represented along the abscissa, and the resulting cochlear potentials are represented along the ordinate. In general, as shown in this graph, the output of the ear rises with sound intensity in a linear fashion until overloading appears and a maximum is reached.7 There- after an increase in stimulus intensity leads to a decrease in cochlear output and the ear is endangered. Any study of this nonlinear portion of the intensity function requires extreme care to prevent serious impairment of the responses. If the pres- entation is kept brief-to bursts of tone of only a second or so-it is often possible to carry the function beyond the maximum, as was done in the example given.

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0.1 /-_FIG. 5.-An intensity function for a tone 0.06 w | j. l Xof 1,000 cps, showing multiple maximums. 0.1 1 10 100 1000 Sound pressure, dynes per sq cm

Here the curve beyond the initial maximum reverses its downward course, rises rapidly, and reaches a new maximum about three times as large as the first. Then for a further increase in stimulation the curve rises to a third maximum, which is nearly ten times as large as the first. Beyond this point only a single measurement could be made because the ear was very rapidly suffering damage. This appearance of successive maximums has been encountered frequently in other lizards, and is sometimes found in mammalian ears as well. An interpretation of this effect has been offered previously,2' 8 but will be repeated here and ex- tended somewhat in view of the unusual complexity shown. This interpretation involves first a considerationi of what a maximum signifies, and secon(l a contempla- tioni of the pattern of action of a tone on the basilar membrane. The recorded potentials represent the combined effects of many hair cells, some of which lie in a region of the basilar membrane where the amplitude of vibration is great and others in neighboring regions where the amplitudes are smaller. A single Downloaded by guest on October 1, 2021 VOIL. 57, 1967 PSYCHOLOGY: WEVER AND HEPP-htEYMOND 685

hair cell evidently produces an output voltage that is a linear function of the amplitude of the movement acting upon it, and then as this amplitude is increased the cell ultimately passes into nonlinearity, reaches a maximum output, and beyond the maximum gives smaller outputs for further stimulus increments. A maximum in the total function, as recorded by an electrode, represents the point at which there is a balance between the decrements of the cells in the most strongly vibrating region of the basilar membrane where severe overloading exists and the increments of cells still operating linearly or approximately so. When the most strongly stimulated cells become injured to the degree that they no longer enter significantly into the total output, it becomes possible by raising the stimulation to high levels to elicit even larger potentials from the ear than before this injury occurred. This happens because most of the cells now making significant contributions to the total output are operating linearly or are only slightly overloaded. As the stimulus intensity is raised further, however, some of these cells-those most strongly involved in the response patterns now existing- pass through their individual maximums into the decremental phase, and the total function shows a second maximum. On rare occasions, as shown here, even a third rise to a maximum can occur, signifying that a third population of hair cells has been forced to pass from linearity to severe nonlinearity. This phenomenon is comparatively rare because it requires three conditions. The first of these is a careful technique of stimulation that delays the injury process and holds it within bounds. A second condition is a certain resistance to injury on the part of the sensory tissues, and perhaps also an ability to recover promptly from mild injury. These two conditions make the injury sufficiently slow for its progressive stages to be seen in a series of observations. In many animals, and notably in the mammals like guinea pigs and cats, the injury from overstimulation is often so rapid and irrecoverable that it is possible to obtain only the first segment of a response curve containing a single maximum. A third condition for the appearance of complex functions such as the one shown here is the presence of differentiation along the basilar membrane. If there were no differentiation, and a given tone produced the same activity in all hair cells throughout the cochlea, then the intensity function could exhibit only one rise to a maximum and the decline beyond. The presence of multiple maximums is evidence that differentiation exists. There is little doubt that there is a considerable degree of frequency differentiation in the ears of certain of the lizards, especially the geckos. This conclusion was reached on other grounds, and especially from observations of the relations between sensitivity, maximum values of potential, and size of hair-cell populations in a series of lizard species.9' 10 The observation of multiple maximums lends weight to this conclusion. The sensitivity function found in Ptyodactylus hasselquistii has much the same form as in other geckos so far studied. The best sensitivity falls in the region from 700 to 1,000 cps, which is the same as found in Hemnidactylus turcicus, though a little above the regions found in Gelko gecko (300-500 cps) and in Coleonyx variegatus (400-600 cps). The degree of sensitivity in Ptyodactylus hasselquistii exceeds that seen in the other geckos, especially if the comparison is made between the more sensitive animals Downloaded by guest on October 1, 2021 686 PSYCHOLOGY: WEVER AND HEPP-REYMOND PROC. N. A. S.

of the different groups. It seems proper in this kind of comparison to place special weight on the more sensitive animals, because almost all the accidental variations that occur, both in the animals themselves and in the testing procedures, are such as to diminish the recorded acuity. The most sensitive animal of the present group required a stimulus intensity of about 81 db below the reference level of 1 dyne/ cm2 to produce a response of 0.1 microvolt, and the average of the three best animals was 76 db below the reference level. The next most sensitive lizard that we have encountered is Coleonyx variegatus, and for this species the comparable figures are 68 db below the reference level for the most sensitive animal and 60 db below the reference level for the best three. Certain individuals of the Ptyodactylus hasselquistii species attain a surprising degree of auditory acuity as measured by the cochlear potentials, and our group as a whole is superior to other species studied. It is probable that geckos in general use vocalizations in the mating process and very likely also for the holding of territories. In a nocturnal animal, auditory sig- nals have a particular advantage in serving these needs. The question has been raised whether there is a sex difference in auditory capac- ities in the fan-toed gecko. In the course of our study we have kept account of sex in the handling of the results, and have not found any convincing differences. The individual variations apart from sex are fairly large, and in a small sample such as we have here, these will obscure any sex difference of moderate size. We can only conclude from the present results that there is no outstanding difference in the hearing of the two sexes. Sumnmary. -1ieasurements of cochlear potentials were carried out in a series of 15 geckos of the species Ptyodactylus hasselquistii puiseuxi, with attention on the sensitivity of the ears, the efficiency of the middle-ear mechanism, and the variation of cochlear output as a function of sound pressure. The ears of these animals were found to be most sensitive in the region of 700- 1,000 cycles per second, which is fairly similar to the forms of sensitivity functions seen in other gecko species. The degree of sensitivity exhibited is outstanding- the best so far seen in any lizard ear. The observation of intensity functions containing multiple maximums is in- terpreted as indicating the presence of frequency differentiation ill terms of place along the basilar membrane. This conclusion is consistent with other recent evi- deuice indicating that in the lizards there has been a progressive development of structure making possible in the more advanced types a discrimination of tones by the place principle. * This investigationwas supported by grants from the National Institute of Neturological Diseases anid Blindness, U.S. Public Health Service, aided by a contract with the Office of Naval Research and by Higgins funds allotted to Princeton University. Permission is granted for reproduction and use by the United States Government. I Wever, E. G., J. A. Vernon, E. A. Peterson, and D. E. Crowley, "Auditory responses in the Tokay gecko," these PROCEEDINGS, 50, 806-811 (1963). 2 Wever, E. G., E. A. Peterson, D. E. Crowley, and J. A. Vernon, "Further studies of hearing in the gekkonid lizards," these PROCEEDINGS, 51, 561-567 (1964). 3 Wever, E. G., D. E. Crowley, and E. A. Peterson, "Auditory sensitivity in four species of lizards," J. Auditory Res., 3, 151-157 (1963). 4 Wever, E. G., and E. A. Peterson, "Auditory sensitivity in three iguanid lizards," J. Auditory Res., 3, 205-212 (1963). Downloaded by guest on October 1, 2021 VOL. 57, 1967 PSYCHOLOGY: WEVER AND HEPP-REYAIOND 687

6 Crowley, D. E., "Auditory responses in the alligator lizard," J. Auditory Res., 4, 135-143 (1964). 6 Wever, E. G., M-C. Hepp-Reymond, and J. A. Vernon, "Vocalization and hearing in the leopard lizard," these PROCEEDINGS, 55, 98-106 (1966). 7Under certain conditions the function fails to exhibit the initial linearity. One condition is the presence of noise, as demonstrated earlier (ref. 2). Another condition, present in Gekko gecko and still incompletely understood, gives rise to nonlinearity and second-harmonic distortion at all levels of stimulation, especially for low and middle frequencies. The second-harmonic distortion is possibly due to the presence of two types of hair-cell stimulation: Hepp-Reymond, M-C., "Patterns in the cochlear potentials of the Tokay gecko (Gekko gecko)," to be published. 8 Wever, E. G., and M. Lawrence, "The patterns of response in the cochlea," J. Acoust. Soc. Am., 21, 127-134 (1949). 9 Wever, E. G., J. A. Vernon, D. E. Crowley, and E. A. Peterson, "Electrical output of lizard ear: relation to hair-cell population," Science, 150, 1172-1174 (1965). 10 Wever, E. G., "Structure and function of the lizard ear," J. Auditory Res., 5, 331-371 (1965). Downloaded by guest on October 1, 2021