Auditory nerve fibre activity in the Tokay gecko - Springer Link

Journal of Comparative Physiology. A

J Comp Physiol (1981) 142:219-226

9 Springer-Verlag 1981

Auditory Nerve Fibre Activity in the Tokay Gecko IL Temperature Effect on Tuning * R.A. Eatock** and G.A. Manley*** Department of Biology, McGill University, 1205 McGregor Ave., Montreal, Quebec, Canada H3A 1B1 Accepted November 5, 1980

Summary. We have recorded from single auditory nerve fibres in the lizard, Gekko gecko, while changing the animal's temperature within the range 19-30 ~ Small steps of 0.5-2 ~ (as measured next to the otic capsule or within the contralateral inner ear) cause a small but reliable and reversible change in the tuning characteristics of a fibre: its tuning curve (frequencythreshold curve) shifts to higher frequencies with warming and lower frequencies with cooling (Figs. 1, 2 and 3). The sharpness of tuning and overall sensitivity of the fibres are relatively unaffected by these procedures. The mean shift in characteristic frequency (CF) for 34 fibres was 0.06 octaves per ~ (Fig. 4A). A more accurate estimate is given by the mean shift in 'centre frequency': a point midway between the low-frequency and high-frequency sides of the tuning curve at 10 dB above CF threshold. This shift was 0.05 octaves per ~ (Fig. 4B), which is equivalent to a thermal Q~0 of approximately 1.4 for the frequency change with temperature. Comparison of these results and analogous frequency shifts with temperature reported for other auditory organs suggests that tuning in the mammalian cochlea is less temperature-dependent than it is in nonmammalian inner ears; this may reflect a basic difference in how tuning is achieved. The observed temperature sensitivities are discussed in terms of what might be expected for tuning by basilar and/or tectorial membranes and for tuning of conductances within the hair cell membrane.

* This work constitutes partial fulfillment of the requirements for the M.Sc. degree of R.A.E. ** Present address: Division of Biology216-76, California Institute of Technology,Pasadena, California 91125, USA *** Present address: Zoologisches Institut der Technischen UniversitS.t Miinchen, Lichtenbergstrasse 4, D-8046 Garching, Federal Republic of Germany Abbreviations." CF characteristic frequency

Introduction One approach in the effort to understand the functioning of the peripheral auditory system has been to study the effects of various perturbations, including temperature change. Early investigations established that in mammals the cochlear microphonic potential (CM) is less sensitive to temperature than are the neural components (N1, N2) of the round-window recording (Coats 1965; Fernandez etal. 1958; Kahana et al. 1950). With hypothermia, N1 and N2 decrease in amplitude and increase in latency, while CM amplitude and latency remain constant down to 5-10 ~ below normal body temperature; further cooling reduces the microphonic but not as much as it reduces the neural components. More recently the summating potential in the mammalian cochlea has been shown to decrease linearly with temperature (Manley and Johnstone 1974). In birds, Necker (1970) found that both CM and summating potential change little with cooling down to 30 ~ below which they decrease in amplitude. Campbell (1969) recorded CM and evoked potentials from the cochlear nuclei in eight lizard species, and found them to be generally most sensitive within the animals' preferred thermal ranges. Werner (1972, 1976) arrived at the same conclusion after studying changes in CM with temperature in iguanids and geckos, but also noted that the frequencies to which the microphonic was most sensitive increased somewhat with temperature. Pursuing this observation, Manley and Werner found that the frequency selectivity (tuning) of individual neurons in the cochlear nuclei of the Tokay gecko also changed with temperature (unpublished data). This unexpected effect interested us as a potential source of information about tuning mechanisms, and seemed to warrant closer study. We chose to record from auditory nerve fibres rather than higher auditory centres, because a temper-

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R.A. Eatock and G.A. Manley: Temperature Effect on Auditory Nerve Fibre Tuning

ature effect on tuning of primary neurons would relate more directly to mechanisms of frequency analysis in the cochlea. The Tokay seemed an appropriate subject since it has sensitive, sharply tuned auditory neurons (Manley 1972; Eatock et al. 1981) and is an ectotherm active over a broad range of temperatures: 20-40 ~ (Werner 1976). Results obtained with temperature changes within this range would presumably not be complicated by adverse effects on the animal's general condition. A preliminary account of some of these data has been reported (Eatock and Manley 1976).

trolled with a thermal control unit accurate to + 0.1 ~ and located outside the sound-attenuating semi-anechoic chamber containing the animal. Glass microelectrodes filled with 3 M KC1 or 4 M NaCl were used to record from that portion of the vestibulocochlear nerve comprising the central processes of the primary auditory neurons. A n auditory unit was identified as such by its time-locked responses to white noise pulses. The procedure upon encountering an auditory fibre was to obtain a frequency-threshold or tuning curve at one temperature, change the temperature and redo the tuning curve. In a number of cases it was possible to repeat these steps several times before contact was lost. The range of temperatures covered by this study was from 19 ~ to 31 ~ Cooling was usually accomplished by simply switching off the heating circuit. In two experiments more rapid, localized cooling was achieved with a gentle stream of cool d a m p air from a small tube connected to an air p u m p and positioned over the exposed braincase and left otic capsule.

Materials and Methods Gekko gecko weighing 40-200 g were imported from Thailand. The data reported in this paper are from 75 auditory nerve fibres in 22 animals; these were the fibres for which it was possible to obtain partial or complete tuning curves at more than one temperature. The surgical approach to the animal's left eighth nerve and the stimulation and recording techniques have been described (Eatock et al. 1981). The animal's temperature was controlled by m e a n s of a heating pad wrapped loosely around its head a n d body. In most experiments, t e m p e r a t u r e was measured with a thermistor probe (6.35 m m diam., 0.06 m m thick) placed in the oral cavity against the right cochlear duct - i.e., contralateral to the exposed auditory nerve. In the last 3 of the 22 experiments, the temperature inside the right cochlear duct was measured with a 24-gauge hypodermic probe. The footplate and part of the columella (stapes) were removed to allow insertion of the probe through the oval window. Temperature was monitored and con-

Results

Since it proved difficult to maintain contact with a given fibre while increasing temperature, two-thirds of the data reported here were obtained while cooling the animal. For 25 of the 75 fibres, tuning curves, or partial tuning curves, were determined at more than two temperatures; three of these fibres were both warmed and cooled. Temperature changes between consecutive curves from a given fibre ranged from 0.3 to 5 ~ but were usually between 0.5 and 1.5 ~ Often temperature changed by up to 1 ~ while an individual tuning curve was being determined; the

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Fig. 1A, B. Temperature effects on the tuning of 2 auditory nerve fibres with CFs around 0.5 kHz. A T u n i n g curves from the same fibre before and after warming the gecko from 22 to 23 ~ (oral temperature). B Tuning curves from a fibre while the animal was being cooled, taken at oral temperatures of 28 a n d 27 ~ Sound pressure levels in this and subsequent figures are in dB re: 20 ~tP

R.A. Eatock and G.A. Manley: Temperature Effect on Auditory Nerve Fibre Tuning 80-

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Fig. 2A, B. Reversibility of the temperature effect. In A, 4 tuning curves were obtained from a fibre while the animal's oral temperature was dropping from 29 to 24.9 ~ After a pause, the same fibre as in A was held while the animal was warmed back up to 28.8 ~ The 3 tuning curves obtained from it during this reheating are shown in B

midpoint of this range was used when comparing the curve with others at different temperatures. The results shown in Fig. 1 are fairly representative: a 1 ~ increase in temperature shifted the tuning curve of the unit in Fig. 1 A toward higher frequencies without greatly affecting the shape of the curve, and a shift in the reverse direction occurred when a unit was cooled (Fig. 1 B). The characteristic frequency (CF) of a unit is that frequency to which it has the lowest threshold; thus, a unit's threshold at CF provides a measure of its overall sensitivity. Although small changes in CF threshold with temperature were common, they were not consistent. There was no tendency for fibres to be more sensitive after either warming or cooling, or at any particular range of temperatures between 19 and 30 ~ Temperature also had no obvious effect on the sharpness of tuning, expressed either as the tuning curves' Q10dB 1 values or as their low-frequency (less than CF) or high-frequency (greater than CF) slopes. Although small changes in sharpness often occurred, these were highly variable. The frequency shift with temperature was reversible, as shown in Fig. 2. The tuning curve of this fibre was determined at four different temperatures while the animal was being cooled, and three more 1 The QloaB of a tuning curve is its CF divided by the bandwidth of the curve at 10 dB above CF threshold

times during reheating. The shifts along the frequency axis during cooling and rewarming were opposite in direction and comparable in magnitude. Between cooling and rewarming there was a pause of several minutes during which response activity was recorded; note that the tuning curve taken before the pause, at 24.9 ~ is almost identical to the one taken several minutes later while temperature was increasing from 24.5 to 25.5 ~ Although more data were obtained from fibres with low characteristic frequencies, the effects were similar for higher-frequency units (Fig. 3). The results in this figure were obtained by cooling for 30 s with a stream of air, as described in Methods. To test whether the noise of the airstream could have contributed to the increased CF thresholds of these units at the lower temperatures, two other units were subjected to 30 s of continuous white noise while temperature was held constant. CF sensitivity was reduced by about 5 dB; no frequency shift occurred. In Fig. 3 then, the frequency shifts but not the threshold changes are probably reliable. Although cooling by this method was much faster than that achieved by simply turning off the heating pad, the resultant frequency shifts were not conspicuously larger, so that the rate of temperature change may not be important. As might be expected, temperature changes measured with the intracochlear thermistor probe lagged somewhat behind simultaneous measurements with the


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oral probe, but the tuning curve shifts per ~ were similar for the two sets of measurements. One way to summarize the shifts in tuning with temperature is simply to plot changes in the fibres' CFs as octave shifts per ~ Fig. 4A shows that CF changes were not always observed, but those that did occur were always in the same direction: toward highe r frequencies with warming and lower frequencies with cooling. The problem with this approach is that it looks at changes in only one point on the tuning curve, and the error associated with any single point may be significant relative to the small frequency shifts under study. A better assessment of the temperature effect can be obtained by considering the shift in a point calculated from all the frequencythreshold values making up the tuning curve. The results of such an analysis are plotted in Fig. 4B, as changes in 'centre frequency' per ~ To obtain the centre frequency of each tuning curve, linear regressions were done on the data points constituting each a r m of the curve. Using the best-fitting lines determined in this way, the tuning curve was redrawn as a simple ' V ' (see inset in Fig. 4B). The shifts with temperature of the low-frequency and high-frequency arms of each ' V ' did not differ significantly. It was therefore reasonable to combine the data from both arms of a given curve by considering only the shift in 'centre frequency', here defined as the frequency midway between the low- and high-frequency regres-

sion lines, at a point 10 dB above CF threshold. Comparison of Figs. 4A and 4 B shows that although the mean shifts in CF and centre frequency were close (0.06 and 0.05 octaves per ~ respectively), the values for the latter showed much less scatter, falling almost entirely between 0.01 and 0.1 octaves per ~ The two high values, + 0 . 4 and +0.6 octaves per ~ in Fig. 4B, were obtained from consecutive units in one animal; the measured temperature changes were from 24 to 23 ~ and from 22 to 23 ~ respectively. These values are inconsistent with the majority, including values at similar CFs and temperatures, even in the same animal. Error in the notation or measurement of temperature or threshold intensities provides the simplest explanation for these two points, and we have excluded them from the calculations that follow. For comparison with other temperature-dependent processes, the frequency shift/~ can be ex~ pressed as a thermal Qlo value, where Qlo is the centre frequency, ft, divided by the centre frequency f t - l o at a temperature 10 ~ colder. It is calculated for smaller temperature shifts,

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R.A. Eatock and G.A. Manley: Temperature Effect on Auditory Nerve Fibre Tuning 0.6

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Fig. 4A, B. Changes in A CF and B 'centre frequency' with temperature. Triangles and circles represent shifts caused by temperature increases and decreases, respectively. Inset in B shows schematically how centre frequency (arrow) was determined for each tuning curve; see text for description. In both A and B results obtained with temperature changes ranging from 0.4 to 4.5 ~ have all been standardized to 'octave shift per ~ and plotted against the units' initial CFs - i.e., for each fibre, the CF of the first tuning curve determined. Plotted in A are 35 shifts from 34 fibres, and in B, 32 shifts from 31 fibres. Although most of the points in the two graphs are from the same raw data, there were several fibres for which the shift in either CF or centre frequency, but not both, could be calculated. Although for many fibres tuning curve shifts were obtained for more than one temperature change, we have plotted only one shift per fibre (except for the fibre of Fig. 2, for which shifts in both directions are plotted). For each unit we compared the two tuning curves that were determined most precisely and/or were separated by the largest temperature shift, since inaccuracy in temperature measurement would most affect the smallest shifts. In calculating the mean frequency shifts, the two very large values at 0.5 kHz were excluded. Mean CF shift (n:33) was 0.06 octaves per ~ mean shift in centre frequency (n=30) was 0.05 octaves per~

Discussion The frequency shift with t e m p e r a t u r e that we have described for a u d i t o r y nerve fibres u n d o u b t e d l y reflects a shift in the t u n i n g o f hair cell receptor potentials, from the following observations. Firstly, that hair cell responses are t u n e d as sharply as those o f p r i m a r y n e u r o n s has been s h o w n in guinea pig (Russell a n d Sellick 1978) a n d turtle (Fettiplace a n d Crawford 1978) a n d is likely to be generally true. Secondly, the specific n a t u r e o f the t e m p e r a t u r e effect - a shift in the frequency d o m a i n a n d its low t h e r m a l Qlo

suggest that t e m p e r a t u r e directly affects the t u n i n g mechanism(s). I n a d d i t i o n the cochlear m i c r o p h o n i c , which is a n extracellular measure o f receptor potentials, undergoes a n a n a l o g o u s frequency shift with t e m p e r a t u r e in the T o k a y ( W e r n e r 1976). I n fact, analysis of W e r n e r ' s C M f u n c t i o n s indicates that the frequency to which the T o k a y ' s C M is most sensitive changes with a Qt0 of a p p r o x i m a t e l y 1.5, m u c h like the centre frequency of the p r i m a r y fibres. W e r n e r also has d e m o n s t r a t e d that after r e m o v a l o f most o f the columella (middle ear bone), C M in response to direct s t i m u l a t i o n o f the columella footplate shows

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the same temperature dependence as CM recorded w i t h the middle ear intact; thus the middle ear is not implicated in the effect. Comparable temperature effects on peripheral frequency selectivity have been observed in several other species, and the combined data suggest ways in which temperature may exert its influence. For comparison, we shall summarize the effects reported in other animals in terms 'of thermal Q10's calculated from the published data. The mean value for the centre frequency shift in the Tokay, 1.4_+0.1 S.E., agrees well with estimates for auditory nerve fibres in caiman and toad. In caiman, Smolders and Klinke (1977) found that over a range of temperatures and frequencies similar to those of the present study, temperature changes evoked CF shifts with Qlo'S on the order of 1.4 to 1.5. Moffat and Capranica (1976) obtained similar Qlo values for fibres innervating one of the toad's two auditory organs, the amphibian papilla. Curiously, fibres from its other auditory organ, the basilar papilla, were unaffected by temperature decreases as large as 10 ~ Whether the different temperature sensitivities of the two papillae reflect a specific difference in their tuning or a more general difference, e.g., in metabolic requirements, cannot be said; the toad's basilar papilla is also insensitive to anoxia, which would be expected to perturb metabolism and evidently does in the amphibian papilla (Capranica and Moffat 1976, and personal communication). Although one must be careful not to overemphasize Qlo values, there appears to be a real difference in the temperature sensitivity of mammalian and nonmammalian auditory organs. Recording guinea pig CM at 37 ~ and 27 ~ de Brey and Eggermont (1978) found that cooling evoked a basal shift in the microphonic's 'excitation profile' along the cochlear partition. This is in effect a frequency shift in the same direction as the shift in the Tokay, caiman and toad; however, the Q10 of the effect was lower - approximately 1.03 - at least for recording from the high-frequency end of the cochlea. A comparably modest influence of temperature on high-frequency tuning in cat cochlear fibres also has been reported; for a small sample of fibres with CFs all around 20 kHz. Smolders and Klinke (1977 and personal communication) recorded CF shifts of " n o t more than 0.04 octaves per 4 ~ which amounts to a Qlo of 1.07 or less. Although the authors regarded this effect as insignificant, it is comparable to the CM shift observed by de Brey and Eggermont. The bimodal distribution of Q10 values: between 1 and 1.1 in mammals, at least at high frequencies, and between 1.4 and 1.6 in reptiles and amphibians, suggests that temperature affects different processes in the two cases. If true, this would imply that mecha-

nisms of frequency sharpening in mammals differ significantly from those in reptiles and amphibians. To see whether the specific effect of temperature on tuning can provide any clues as to how hair cells are tuned, we shall consider in turn what temperature sensitivity would be expected if 1) the signal input to the hair cells is sharpened by accessory structures within the cochlea, or 2) voltage-sensitive conductances of the cell membrane constitute a tuned system. The mammalian cochlea has at least one tuning mechanism that falls into the first of the two categories listed: the mechanical tuning of the basilar membrane. That this is the site of the temperature effect in mammals has been proposed by de Brey and Eggermont, who suggested that increased compliance of the basilar membrane with cooling could cause the CM shift observed in guinea pig. This is a reasonable possibility; although the composition of the basilar membrane is not known, elastic body tissues (elastomers) in general seem to behave like rubber, becoming less stiff with cooling with a rather low Q10 e.g., 1.1 or less for elastin in vitro (McCrum 1977). However, there is no evidence for sophisticated frequency analysis by the basilar membrane in the Tokay, and it definitely does not occur in the toad, whose auditory papillae rest directly against the wall of the cochlear duct. For these animals it is conceivable that the tectorial membrane assists in tuning and is sensitive to temperature, yet the Q10 values seem large for an effect of the sort suggested for the mammalian basilar membrane. This brings us to the second possibility, that temperature affects a tuned system of membrane conductances in the hair cell. As discussed in the accompanying paper (Eatock et al. 1981), the existence of such a system of conductances has been suggested by evidence that low-frequency hair cells undergo voltage oscillations at their characteristic frequencies either spontaneously or in response to nonspecific perturbations. Some of this evidence is from cells that are homologous to hair cells: certain electroreceptors in weakly electric fish. Intriguingly, the tuning curves of afferents from these organs show frequency shifts with temperature in the same direction as those we have described for auditory afferents (Hopkins 1976) a result that supports the suggestion that these homologous organs may share common tuning mechanisms (Eatock et al. 1981). On the other hand, Hopkins' estimates of thermal Q10 for two electroreceptor afferents were 2.8 and 3 ; if representative, these values may reflect important differences in tuning of electroreceptor and auditory organs. It should also be emphasized that all the evidence for voltage oscillations is for frequencies below about 1 kHz, so that alternate tuning mechanisms


may have to be considered at higher frequencies. The temperature data are not informative in this regard. Figure 4 shows no obvious dichotomy in the temperature sensitivity of low- and high-frequency tuning, but there are too few data points to be certain 2. What would determine the Qlo of the oscillation frequency in the case of the postulated tuned system of membrane channels ? The oscillations might result from a negative feedback loop, as follows: current through activated voltage-sensitive channels would change membrane potential so as to eventually inactivate the channels, then a leak conductance or another set of channels would repolarize the cell, reactivating the first conductance, etc. The temperature sensitivity of the oscillation frequency would depend on the sensitivity of the components that introduce delays into the negative feedback. These components are the membrane time constant, which determines the time required for a given current to change membrane potential a given amount, and channel gating kinetics, which limit the speed with which voltage-sensitive channels can respond to changes in membrane potential. The membrane charging time depends on the ratio of membrane capacitance to conductance. While the temperature dependence of membrane capacitance is negligibly low (Cole 1968), the conductances of membrane channels have Qlo'S that are low but significant: usually about 1.3 (Jack et al. 1975). Thus, where the rate-limiting component of the system is the cell's time constant, one would predict a Q~o for the oscillation frequency of about 1.3. A higher value is expected if channel gating is slow relative to the time taken to charge the membrane, since Qlo'S for channel gating are typically 2-3 (e.g., Anderson and Stevens 1973; Frankenhaeuser and Moore 1963). For example, the squid axon produces oscillatory potentials (200-300 Hz) in response to subthreshold stimulation. The high temperature dependence of the oscillation frequency (Qto = 2.25 ; Guttman 1969) in this system may reflect the slow opening rate of the squid axon's potassium channel, 1-2 ms, relative to its membrane time constant, 0.3 ms at 25 ~ and with the axon slightly depolarized (Hodgkin and Huxley 1952). Although the time constants of hair cells in the Tokay, caiman and toad are not known, they are probably in the same range as estimates from other reptiles and amphibians. Hair cells of the bullfrog sacculus have a time constant close to 10 ms (A.J. Hudspeth, personal communication) while in turtle cochlea, the cell size and amount of injected current needed to reach reversal potential (Crawford and Fet2 Above l kHz, n = 7 and Qlo=1.24+0.06 (mean+standard error). For CFs< 1 kHz, n=23 and mean Qlo = 1.46_+0.53

225

tiplace 1979) indicate a time constant of at least 2 ms. How would a time constant between 2 and 10 ms compare to the kinetics expected for channels involved in the oscillatory potential? The voltage-sensitive potassium channel, the slowest of those likely to be involved, is probably faster than the expected time constant, since the delayed rectification in bullfrog hair cells turns on in 1-2 ms (D.P. Corey, personal communication). Thus in reptiles and amphibians the charging time of the hair cell membrane is likely to be slower than the gating of channels, and so would dominate in setting the frequency of oscillatory receptor potentials. One would predict as a consequence that the temperature dependence of the oscillation frequency in such cells would be closer to that of membrane conductance than that of channel kinetics. The Qlo of the frequency shift in Tokay, caiman and toad, being close to the Q10 for membrane conductance, is therefore consistent with the proposal that oscillatory voltage-sensitive channels in the hair cells form the basis of low-frequency tuning in these systems.

Special thanks are due to D.P. Corey for invaluable discussions and advice. We also thank D.C. Van Essen for comments on the manuscript. This work was supported by grants from the National Research Council of Canada and the Quebec Dept. of Education.

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Frankenhaeuser B, Moore LE (1963) The effect of temperature on the sodium and potassium permeability changes in myelinated nerve fibres of Xenopus taevis. J Physiol 169:431-437 Guttman R (1969) Temperature dependence of oscillatory behavior of squid axons. Biophys J 9:269-277 Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500-544 Hopkins CD (1976) Stimulus filtering and electroreception: tuberous electroreceptors in three species of gymnotoid fish. J Comp Physiol 111:171-207 Jack JJB, Noble D, Tsien RW (1975) Electric current flow in excitable cells, Oxford University Press, London Manley GA (1972) Frequency response of the ear of the Tokay gecko. J Exp Zool 181:159-168 Manley JA, Johnstone BM (1974) A comparison of cochlear summating potentials in the bat and guinea pig, including temperature effects. J Comp Physiol 88:43-66 McCrum NG (1977) The molecular conformation of elastin as derived from mechanical investigations. In~ Sandberg LB, Gray

WR, Franzblau C (eds) Elastin and elastic tissues. Plenum, New York, pp 633-543 Moffat AJM, Capranica RR (1976) Effects of temperature on the response properties of auditory nerve fibers in the American toad (Bufo americanus). J Acoust Soc Am 60 Suppl 1 : 580 Necker R (1970) Zur Entstehung der Cochleapotentiale yon VSgeln: Verhalten bei O2-Mangel, Cyanidvergiftung und Unterktihlung sowie Beobachtungen fiber die diumliche Verteilung. Z Vergl Physiol 69 : 367-425 Russell IJ, Sellick PM (1978) Intracellular studies of hair cells in the mammalian cochlea. J Physiol 284:261-290 Smolders J, Klinke R (1977) Effect of temperature changes on tuning properties of primary auditory fibres in caiman and cat. In: Portmann M, Aran J-M (eds) Inner ear biology. Les colloques de l'institut nationale de la sant~ et de la recherche m~dicale. 68: p 125. INSERM, Paris Werner YL (1972) Temperature effects on inner-ear sensitivity in six species of iguanid lizards. J Herpetol 6:147-177 Werner YL (1976) Optimal temperatures for inner-ear performance in gekkonid lizards. J Exp Zool 195:319-352