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Auditory Sexual Difference in the Large Odorous Frog Odorrana Graminea

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Auditory Sexual Difference in the Large Odorous Frog Odorrana Graminea J Comp Physiol A (2014) 200:311–316 DOI 10.1007/s00359-014-0885-3 ORIGINAL PAPER Auditory sexual difference in the large odorous frog Odorrana graminea Wei-Rong Liu · Jun-Xian Shen · Yu-Jiao Zhang · Zhi-Min Xu · Zhi Qi · Mao-Qiang Xue Received: 8 August 2013 / Revised: 15 January 2014 / Accepted: 22 January 2014 / Published online: 9 February 2014 © Springer-Verlag Berlin Heidelberg 2014 Abstract Acoustic communication is an important Abbreviations behavior in frog courtship. Male and female frogs of most AENFP Auditory evoked near-field potential species, except the concave-eared torrent frog Odorrana BEF Best excitatory frequency tormota, have largely similar audiograms. The large odorous CF Characteristic frequency frogs (Odorrana graminea) are sympatric with O. tormota, RMS Root mean square but have no ear canals. The difference in hearing between SPL Sound pressure level two sexes of the frog is unknown. We recorded auditory TS Torus semicircularis evoked near-field potentials and single-unit responses from the auditory midbrain (the torus semicircularis) to deter- mine auditory frequency sensitivity and threshold. The Introduction results show that males have the upper frequency limit at 24 kHz and females have the upper limit at 16 kHz. The Acoustic communication is often associated with the more sensitive frequency range is 3–15 kHz for males and behaviors of frogs, including territorial behavior, mate 1–8 kHz for females. Males have the minimum threshold at finding, courtship and aggression (Zelick et al. 1999). Dur- 11 kHz (58 dB SPL), higher about 5 dB than that at 3 kHz ing the breeding season, an adult male usually produces for females. The best excitatory frequencies of single units advertisement calls to attract receptive female to the calling are mostly between 3 and 5 kHz in females and at 7–8 kHz male, followed by courtship, leading to amplexus. in males. The underlying mechanism of auditory sexual However, a sex difference in the peripheral auditory sen- differences is discussed. sitivity was observed in the American bullfrog (Rana cates- beiana) (Hetherington 1994; Mason et al. 2003) and in the Keywords Auditory evoked near-field potential · tree frog (Eleutherodactylus coqui) (Narins and Capranica Auditory threshold · Sex difference · Frogs · Torus 1976). A recent study through behavioral and physiologi- semicircularis cal experiments and laser Doppler vibrometer measure- ments demonstrated that the concave-eared torrent frogs (Odorrana tormota) have significant sexual differences in auditory frequency sensitivity (Shen et al. 2011a). Males of O. tormota have the ultrasonic communication capacity, W.-R. Liu · Y.-J. Zhang · Z. Qi · M.-Q. Xue but females exhibit no ultrasonic sensitivity. It appears that Department of Basic Medical Sciences, Medical College ultrasonic components in male’s calls might be not essen- of Xiamen University, Xiamen 361102, China e-mail: [email protected] tial to attract female approaching during courtship. The large odorous frog (Odorrana graminea, previously J.-X. Shen (*) · Z.-M. Xu O. livida) is an arboreal and nocturnal species sympatric State Key Laboratory of Brain and Cognitive Science, Institute with O. tormota living in the Huangshan Hot Spring area, of Biophysics, Chinese Academy of Sciences, Beijing 100101, China China. Males of O. graminea produce diverse types of e-mail: [email protected] calls, most of them containing ultrasonic harmonics (Shen 1 3 312 J Comp Physiol A (2014) 200:311–316 et al. 2011b). A preliminary study indicated that males of reading RMS). Each stimulus at different frequencies O. graminea have the ability to hear ultrasound (Feng et al. was modulated relative to 90 dB SPL using a Program- 2006). It is unclear whether males communicate with ultra- mable Attenuator (PA5, TDT) and the BrainWare software sound and females detect ultrasound as well. (distributed by TDT). The stimulus presentation and data To explore the auditory sexual difference, we recorded acquisition were done in an automated mode with the auditory evoked near-field potentials (AENFP) and single- BrainWare. unit responses from the torus semicircularis (TS) of mid- brain in O. graminea. The findings indicate that males have Neurophysiology ultrasonic communication capacity and females are insensi- tive to ultrasound. Glass microelectrodes filled with 3 M sodium acetate (impedances 1–10 MΩ) were used to record AENFPs or single-unit spikes induced by tone bursts (frequency range Materials and methods 1–30 kHz) from the frog’s TS. An indifferent electrode was placed at the nearby muscles. The first site for microelec- Animals trode was located at the dorsal surface of the torus away from the midline of the brain about 1.0 mm, then orthogo- Thirty-four male and eight female frogs of O. graminea nally inserted into the surface of the TS by a remote-con- (Boulenger) were collected in the Huangshan Hot Spring trolled Pulse Motor Micro-Drive Micromanipulator (SM- area, China in May and June of 2009 and 2011, and carried 21, Narishige, Tokyo, Japan) with an accuracy of 1 μm. into the Institute of Biophysics in Beijing for electrophysi- Neurons were identified along the penetration track by their ological study. The methods were similar to those described responses to sound in various sound pressure levels for all in the previous papers (Feng et al. 2006; Shen et al. 2011a) frequencies. A subsequent penetration site for electrode with slight modifications. Briefly, frogs were lightly anes- was placed caudo-rostrally or medial-laterally about 50 μm thetized by immersed in a 0.2 % solution of tricaine meth- away from the preceding site. A lower band-pass filter anesulfonate (MS222) for 2–5 min. After anesthesia, the (20–200 Hz) was used for AENFP recordings and single- animal body was wrapped in cotton gauze and the head was unit responses were band-pass filtered between 300 Hz and unwrapped to make the sound transmission uninterrupted. 3 kHz. Neural signals were recorded by RA4PA Preamp To immobilize the frog, the jaw and hind limbs of the frog and RA16 Medusa Base (TDT), monitored visually and were pinned on a platform made from paraffin. The skin on extracted using BrainWare and stored on a hard drive. the dorsal surface of the head was incised, and a small hole AENFP measured from each recording site was averaged was made in the skull above the TS. During the record- over 20 trials at corresponding sound pressure levels across ing session, the frog was placed on a vibration-free plat- frequencies. The amplitude and latency of all AENFPs form inside a sound-proof and anechoic room with periodic from one recording site were read out from digital infor- addition of 0.1 % MS222 to keep the frog in light anesthe- mation of their waveforms by the BrainWare, forming a sia. The temperature was maintained at 19–21 °C by an air dataset, in which the maximum peak-to-peak amplitude of conditioner. AENFPs was as 100 %, amplitudes of other AENFPs were normalized. The threshold for AENFP at a frequency is the Sound signals minimum sound pressure level of a stimulus as the point at which the amplitude of AENFP is equal to or greater than Sound signals were generated by an RP2.1 Enhanced 120 % of the amplitudes of other waves. The threshold for Real-time Processor [Tucker Davis Technologies (TDT) single unit is the minimum sound pressure level of a stimu- System 3, USA] and amplified via a power amplifier (GF- lus as the point at which spike activity of certain latency is 10, China), and broadcasted from the loudspeaker (fre- elicited at least three times per 10 stimuli. A total of 74 sets quency range 1–30 kHz; FE87E, Fostex, Japan) placed of AENFPs were measured from 8 females and 114 sets at a distance of 50 cm from the frog’s eardrum on the of AENFPs measured from 34 males, and the single-unit side contralateral to the recording site in the TS. Acous- spike activities were measured from 3 females (47 units) tic stimuli consisted of tone bursts (50-ms duration, 5-ms and 15 males (81 units). rise and fall times, presented at a rate of 1/s). The sound pressure levels of the stimulation system were measured Data analysis using a condenser microphone (Brüel and Kjaer 4135, Denmark) placed at the position corresponding to the The results were presented as mean SE. The Origin 7.0 ± frog’ eardrum and a precision measuring amplifier (Brüel (Originlab, Northampton, MA, USA) and one-way ANOVA and Kjaer 2610, Denmark) in dB SPL (re. 20 μPa) (fast were used for statistical analyses and plotting graphs. 1 3 J Comp Physiol A (2014) 200:311–316 313 Fig. 1 Auditory evoked near- field potentials measured from the torus semicircularis of the midbrain in O. graminea. The AENFP waveforms were recorded and averaged from a female (a) and a male (c) in response to 20 bursts presented at frequency range of 1–24 kHz at 90 dB SPL and rate of 1/s. Lines with different colors represent different tone fre- quency shown in the right color palette. b and d Peak-to-peak amplitude (black) and response latency (blue) of the AENFPs are depicted as a function of tone frequency, respectively, corresponding to a and c Results value of the peak ranged from 1 to 7 kHz for females, while from 2 to 9 kHz (or even 13 kHz) for males. Statistic analy- Auditory evoked near-field potentials from TS sis indicates significant difference in the AENFP amplitude versus frequency relationship between the two sexes at all The AENFPs recorded from the TS of a female and a tested frequencies [one-way ANOVA with Bonferroni cor- male of O. graminea are shown in Fig. 1a, c, respectively.
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