Abstract
During metamorphosis, the lateral line system of ranid frogs (Rana catesbeiana) degenerates and an auditory system sensitive to airborne sounds develops. We examined the onset of function and developmental changes in the central auditory system by recording multi-unit activity from the principal nucleus of the torus semicircularis (TSp) of bullfrogs at different postmetamorphic stages in response to tympanically-presented auditory stimuli. No responses were recorded to stimuli of up to 95 dB SPL from latemetamorphic tadpoles, but auditory responses were recorded within 24 hours of completion of metamorphosis. Audiograms from froglets (SVL < 5.5 cm) were relatively flat in shape with high thresholds, and showed a decrease in most sensitive frequency (MSF) from about 2500 Hz to about 1500 Hz throughout the first 7–10 days after completion of metamorphosis. Audiograms from frogs larger than 5.5 cm showed continuous downward shifts in MSF and thresholds, and increases in sharpness around MSF until reaching adult-like values. Spontaneous activity in the TSp increased throughout postmetamorphic development. The torus increased in volume by approximately 50% throughout development and displayed changes in cell density and nuclear organization. These observations suggest that the onset of sensitivity to tympanically presented airborne sounds is limited by peripheral, rather than central, auditory maturation.
Similar content being viewed by others
Abbreviations
- CF :
-
characteristic frequency
- MSF :
-
most sensitive frequency
- PB :
-
phasic burst
- PL :
-
primary like
- S :
-
sustained
- SVL :
-
snout-vent length
- TS :
-
torus semicircularis
- TSl :
-
laminar nucleus of TS
- TSm :
-
magnocellular nucleus of TS
- TSp :
-
principal nucleus of TS
- TW :
-
tympanic width
References
Aitkin LM, Moore DR (1975) Inferior colliculus. II. Development of tuning characteristics and tonotopic organization in central nucleus of the neonatal cat. J Neurophysiol 38: 1208–1216
Capranica RR (1965) The evoked vocal response of the bullfrog: A study of communication by sound. MIT Press, Cambridge MA
Capranica RR (1976) Morphology and physiology of the auditory system. In: Llinas R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 443–466
Corse WA, Metter DE (1980) Economics, adult feeding and larval growth of Rana catesbeiana on a fish hatchery. J Herpetol 14: 231–238
Corwin JT (1985) Perpetual production of hair cells and maturational changes in hair cell ultrastructure accompany postembryonic growth in an amphibian ear. Proc Natl Acad Sci USA 82: 3911–3915
Ehret G, Tautz J, Schmitz B, Narins PM (1990) Hearing through the lungs: Lung-eardrum transmission of sound in the frog Eleutherodactylus coqui. Naturwissenschaften 77: 192–194
Feng AS, Lin W (1991) Differential innervation patterns of three divisions of frog auditory midbrain (Torus semicircularis). J Comp Neurol 306: 613–630
Frishkopf LS, Capranica RR, Goldstein MH (1968) Neural coding in the bullfrog's auditory system — a teleological approach. Proc IEEE 56: 969–980
Fritzsch B, Nikundiwe AM, Will U (1984) Projection patterns of lateral-line afferents in anurans: A comparative HRP study. J Comp Neurol 229: 451–469
Fritzsch B, Wahnschaffe U, Bartsch U (1988) Metamorphic changes in the octavolateralis system of amphibians. In: Fritzsch B, Ryan M, Wilczynski W, Hetherington TE, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 359–376
Gooler DM, Feng AS (1992) Temporal coding in the frog auditory midbrain: The influence of duration and rise-fall time on the processing of complex amplitude-modulated stimuli. J Neurophysiol 67: 1–22
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183–190
Hanken J (1989) Development and evolution in amphibians. Am Sci 77: 336–343
Hetherington TE (1987) Timing of development of the middle ear of Anura (Amphibia). Zoomorphology 106: 289–300
Hetherington TE (1992) The effects of body size on functional properties of middle ear systems of anuran amphibians. Brain Behav Evol 39: 133–142
Hetherington TE (1994) Sexual differences in the tympanic frequency responses of the American bullfrog (Rana catesbeiana). J Acoust Soc Am 96: 1186–1188
Huangfu M, Saunders JC (1983) Auditory development in the mouse: Structural maturation of the middle ear. J Morphol 176: 249–259
Hughes A (1976) Metamorphic changes in the brain and spinal cord. In: Llina R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 856–862
Jacoby J, Rubinson K (1983) The acoustic and lateral line nuclei are distinct in the premetamorphic frog, Rana catesbeiana. J Comp Neurol 216: 152–161
Jacoby J, Rubinson K (1984) Efferent projections of the torus semicircularis to the medulla of the tadpole, Rana catesbeiana. Brain Res 292: 378–381
Larsell O (1934) The differentiation of the peripheral and central acoustic apparatus in the frog. J Comp Neurol 39: 473–527
Li CW, Lewis ER (1974) Morphogenesis of auditory receptor epithelia in the bullfrog. In: Johari O, Corvin I (eds) Scanning electron microscopy. IIT Res Inst, Chicago, pp 791–798
Lippe WR (1987) Shift of tonotopic organization in brain stem auditory nuclei of the chicken during late embryonic development. Hearing Res 25: 205–208
Lippe WR (1994) Rhythmic spontaneous activity in the developing avian auditory system. J Neurosci 14: 1486–1495
Lippe WR, Rubel EW (1985) Ontogeny of tonotopic organization of brain stem auditory nuclei in the chicken: implications for development of the place principle. J Comp Neurol 237: 273–289
Lombard RE, Fay RR, Werner YL (1981) Underwater hearing in the frog, Rana catesbeiana. J Exp Biol 91: 57–71
Luschekin VS, Luschekina EA, Skuleikina KV (1992) Features of the establishment of the spontaneous activity of neurons of the trigeminal sensory nuclei of viable sections of the rat brainstem in postnatal ontogenesis. Neurosci Behav Physiol 22: 45–50
Megela AL, Capranica RR (1983) A neural and behavioral study of auditory habituation in the bullfrog, Rana catesbeiana. J Comp Physiol 151: 423–434
Megela-Simmons A, Moss CF, Daniel KM (1985) Behavioral audiograms of the bullfrog (Rana catesbeiana) and the green tree frog (Hyla cinerea). J Acoust Soc Am 78: 1236–1244
Moore DR, Irvine DF (1979) The development of some peripheral and central auditory responses in the neonatal cat. Brain Res 163: 49–59
Nakamura S, Kimura F, Sakaguchi T (1987) Postnatal development of electrical activity in the locus ceruleus. J Neurophysiol 58: 510–524
Narins PM, Lewis ER (1984) The vertebrate ear as an exquisite seismic sensor. J Acoust Soc Am 76: 1384–1387
Narins PM, Ehret G, Tautz J (1988) Accessory pathway for sound transfer in a neotropical frog. Proc Natl Acad Sci USA 85: 1508–1512
Playford DE, Dunlop SA (1993) A biphasic sequence of myelination in the developing optic nerve of the frog. J Comp Neurol 333: 83–93
Potter HD (1965) Mesencephalic auditory region of the bullfrog. J Neurophysiol 28: 1132–1154
Rebillard G, Rubel EE (1981) Electrophysiological study of maturation of auditory responses from the inner ear of the chick. Brain Res 229: 15–23
Romand R (1987) Tonotopic evolution during development. Hearing Res 28: 117–123
Romand R, Ehret G (1990) Development of tonotopy in the inferior colliculus. I. Electrophysiological mapping in house mice. Dev Brain Res 54: 221–234
Rubel EW, Ryals B (1983) Development of the place principle: Acoustic trauma. Science 219: 512–514
Rübsamen R (1992) Postnatal development of central auditory frequency maps. J Comp Physiol A 170: 129–143
Rübsamen R, Neuweiler G, Marimuthu G (1989) Ontogenesis of tonotopy in inferior colliculus of a hipposiderid bat reveals postnatal shift in frequency-place code. J Comp Physiol A 165: 755–769
Sedra SN, Michael MI (1959) The ontogenesis of the sound conducting apparatus of the Egyptian toad Bufo regularis Reuss, with a review of this apparatus in Salientia. J Morph 104: 359–375
Shofner WP, Feng AS (1981) Post-metamorphic development of the frequency selectivities and sensitivities of the peripheral auditory system of the bullfrog, Rana catesbeiana. J Exp Biol 93: 181–196
Shofner WP, Feng AS (1984) Quantitative light and scanning electron microscopic study of the developing auditory organs in the bullfrog: Implications on their functional characteristics. J Comp Neurol 224: 141–154
Stehouwer DJ (1988) Metamorphosis of behavior in the bullfrog (Rana catesbeiana). Dev Psychobiol 21: 383–395
Stiebler IB, Narins PM (1990) Temperature-dependence of auditory nerve response properties in the frog. Hearing Res 46: 63–82
Thomas JP, Walsh EJ (1990) Postnatal development of the middle ear: areal ratios in kittens. Otolaryngol Head Neck Surg 103: 427–535
van Dijk P, Lewis ER, Wit HP (1990) Temperature effects on auditory nerve fiber response in the American bullfrog. Hearing Res 44: 231–240
Wassersug RJ (1973) Aspects of social behavior in anuran larvae. In: Vial JL (ed) Evolutionary biology of anurans. Univ Missouri Press, Columbia MO, pp 273–297
Wever EG (1985) The amphibian ear. Princeton Univ Press, Princeton NJ
Wilczynski W, Zakon HH, Brenowitz EA (1984) Acoustic communication in spring peepers: Call characteristics and neurophysiological aspects. J Comp Physiol A 155: 577–584
Wilczynski W, Resler C, Capranica RR (1987) Tympanic and extratympanic sound transmission in the leopard frog. J Comp Physiol A 161: 659–669
Witschi E (1949) The larval ear of the frog and its transformation during metamorphosis. Z Naturforsch 4b: 230–242
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Boatright-Horowitz, S.S., Simmons, A.M. Postmetamorphic changes in auditory sensitivity of the bullfrog midbrain. J Comp Physiol A 177, 577–590 (1995). https://doi.org/10.1007/BF00207187
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00207187