Skip to main content
SpringerLink
Log in

“To Ear is Human, to Frogive is Divine”: Bob Capranica’s legacy to auditory neuroethology

  • Review
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Bob Capranica was a towering figure in the field of auditory neuroethology. Among his many contributions are the exploitation of the anuran auditory system as a general vertebrate model for studying communication, the introduction of a signal processing approach for quantifying sender–receiver dynamics, and the concept of the matched filter for efficient neural processing of complex vocal signals. In this paper, meant to honor Bob on his election to Fellow of the International Society for Neuroethology, I provide a description and analysis of some of his most important research, and I highlight how the concepts and data he contributed still inspire neuroethology today.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AP:

Amphibian papilla

AM:

Amplitude modulation

ACF:

Autocorrelation function

BP:

Basilar papilla

CF:

Characteristic frequency

IC:

Inferior colliculus

ICN:

International Congress of Neuroethology

PRR:

Pulse repetition rate

TS:

Torus semicircularis

References

  • Amézquita A, Flechas SV, Lima AP, Gasser H, Hodl W (2011) Acoustic interference and recognition space within a complex assemblage of dendrobatid frogs. PNAS 108:17058–17063

    Article  PubMed  Google Scholar 

  • Bodnar DA, Capranica RR (1994) Encoding of phase spectra by the peripheral auditory system of the bullfrog. J Comp Physiol A 174:157–171

    Article  PubMed  CAS  Google Scholar 

  • Capranica RR (1965) The evoked vocal response of the bullfrog: a study of communication by sound. MIT Press, USA

    Google Scholar 

  • Capranica RR (1983) Sensory processing of key stimuli. In: Ewert JP, Capranica RR, Ingle D (eds) Advances in vertebrate neuroethology. Plenum Press, New York, pp 3–6

    Chapter  Google Scholar 

  • Capranica RR (1992) The untuning of the tuning curve: is it time? Sem Neurosci 4:401–408

    Article  Google Scholar 

  • Capranica RR, Moffat AJM (1975) Selectivity of the peripheral auditory system of spadefoot toads (Scaphiopus couchi) for sounds of biological significance. J Comp Physiol 100:231–249

    Article  Google Scholar 

  • Capranica RR, Moffat AJM (1980) Nonlinear properties of the peripheral auditory system of anurans. In: Popper AN, Fay RR (eds) Comparative studies of hearing in vertebrates. Springer, New York, pp 139–165

    Chapter  Google Scholar 

  • Capranica RR, Moffat AJM (1983) Neurobehavioral correlates of sound communication in anurans. In: Ewert JP, Capranica RR, Ingle D (eds) Advances in vertebrate neuroethology. Plenum Press, New York, pp 701–730

    Chapter  Google Scholar 

  • Capranica RR, Frishkopf LS, Nevo E (1973) Encoding of geographic dialects in the auditory system of the cricket frog. Science 182:1272–1275

    Article  PubMed  CAS  Google Scholar 

  • Ehret G, Capranica RR (1980) Masking patterns and filter characteristics of auditory nerve fibers in the green tree frog (Hyla cinerea). J Comp Physiol 141:1–12

    Article  Google Scholar 

  • Ehret G, Moffat AJ, Capranica RR (1983) Two-tone suppression in auditory nerve fibers of the green treefrog (Hyla cinerea). J Acoust Soc Am 73:2093–2095

    Article  PubMed  CAS  Google Scholar 

  • Elliott TM, Christensen-Dalsgaard J, Kelley DB (2007) Tone and call responses of units in the auditory nerve and dorsal medullary nucleus of Xenopus laevis. J Comp Physiol A 193:1243–1257

    Article  Google Scholar 

  • Elliott TM, Christensen-Dalsgaard J, Kelley DB (2011) Temporally selective processing of communication signals by auditory midbrain neurons. J Neurophysiol 105:1620–1632

    Article  PubMed  Google Scholar 

  • Ewert JP, Capranica RR, Ingle D (1983) Advances in vertebrate neuroethology. Plenum Press, New York

    Book  Google Scholar 

  • Feng AS, Narins PM, Capranica RR (1975) Three populations of primary auditory fibers in the bullfrog (Rana catesbeiana): their peripheral origins and frequency sensitivities. J Comp Physiol 100:221–229

    Article  Google Scholar 

  • Feng AS, Hall JC, Gooler DM (1990) Neural basis of sound pattern recognition in anurans. Prog Neurobiol 34:313–329

    Article  PubMed  CAS  Google Scholar 

  • Ferragamo MJ, Haresign T, Simmons JA (1998) Frequency tuning, latencies, and responses to FM sweeps in the inferior colliculus of the echolocating bat, Eptesicus fuscus. J Comp Physiol A 182:65–79

    Article  PubMed  CAS  Google Scholar 

  • Freedman EG, Ferragamo M, Simmons AM (1988) Masking patterns in the bullfrog (Rana catesbeiana). II: physiological effects. J Acoust Soc Am 84:2081–2091

    Article  PubMed  CAS  Google Scholar 

  • Frishkopf LS, Capranica RR, Goldstein MH (1968) Neural coding in the bullfrog’s auditory system—a teleological approach. Proc IEEE 56:969–980

    Article  Google Scholar 

  • Fuzessery ZM, Feng AS (1982) Frequency selectivity in the anuran auditory midbrain: single unit responses to single and multiple tone stimulation. J Comp Physiol 146:471–484

    Article  Google Scholar 

  • Fuzessery ZM, Feng AS (1983) Mating call selectivity in the thalamus and midbrain of the leopard frog (Rana p. pipiens): single and multiunit analysis. J Comp Physiol 150:333–344

    Article  Google Scholar 

  • Gentner TQ, Margoliash D (2002) The neuroethology of vocal communication: perception and cognition. In: Simmons AM, Popper AN, Fay RR (eds) Acoustic communication. Springer, New York, pp 324–386

    Google Scholar 

  • Gerhardt HC, Schwartz JJ (2001) Auditory tuning and frequency preferences in anurans. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington DC, pp 73–85

    Google Scholar 

  • Hainfeld C, Boatright-Horowitz SL, Boatright-Horowitz SS, Simmons AM (1996) Discrimination of phase spectra in complex sounds by the bullfrog, Rana catesbeiana. J Comp Physiol A 178:75–87

    Google Scholar 

  • Hillery CM, Narins PM (1987) Frequency- and time-domain comparison of low-frequency auditory fiber responses in two anuran amphibians. Hear Res 25:233–248

    Article  PubMed  CAS  Google Scholar 

  • Hoke KL, Burmeister SS, Fernald RD, Rand AS, Ryan MJ, Wilczynski W (2004) Functional mapping of the auditory midbrain during mate call reception. J Neurosci 24:11264–11272

    Article  PubMed  CAS  Google Scholar 

  • Ladich F (2000) Acoustic communication and the evolution of hearing in fishes. Phil Trans R Soc Lond B 355:1285–1288

    Article  CAS  Google Scholar 

  • Langner G (1992) Periodicity coding in the auditory system. Hear Res 60:115–142

    Article  PubMed  CAS  Google Scholar 

  • Langner G, Schreiner C (1988) Periodicity coding in the inferior colliculus of the cat I. Neuronal mechanisms. J Neurophysiol 60:1799–1822

    PubMed  CAS  Google Scholar 

  • Lombard RE, Straughan IR (1974) Functional aspects of anuran middle ear structures. J Exp Biol 61:57–71

    Google Scholar 

  • Meddis R, Hewitt MJ (1991) Virtual pitch and phase-sensitivity studied using a computer model of the auditory periphery: II phase sensitivity. J Acoust Soc Am 89:2883–2894

    Article  Google Scholar 

  • Megela AL (1983) Auditory response properties of the anuran diencephalon: nonlinear facilitation. In: Ewert JP, Capranica RR, Ingle D (eds) Advances in vertebrate neuroethology. Plenum Press, New York, pp 895–899

    Chapter  Google Scholar 

  • Megela AL (1984) Diversity of adaptation patterns in responses of eighth nerve fibers in the bullfrog, Rana catesbeiana. J Acoust Soc Am 75:1115–1162

    Article  Google Scholar 

  • Megela AL, Capranica RR (1981) Response patterns to tone bursts in peripheral auditory system of anurans. J Neurophysiol 46:465–478

    PubMed  CAS  Google Scholar 

  • Megela AL, Capranica RR (1982) Differential patterns of physiological masking in the anuran auditory nerve. J Acoust Soc Am 71:641–645

    Article  PubMed  CAS  Google Scholar 

  • Moss CF, Simmons AM (1986) Frequency selectivity of hearing in the green treefrog, Hyla cinerea. J Comp Physiol A 159:257–266

    Article  PubMed  CAS  Google Scholar 

  • Mudry KM, Capranica RR (1987a) Correlation between auditory evoked responses in the thalamus and species-specific call characteristics. I. Rana catesbeiana (Anura: Ranidae). J Comp Physiol A 160:477–489

    Article  PubMed  CAS  Google Scholar 

  • Mudry KM, Capranica RR (1987b) Correlation between auditory thalamic area evoked responses and species-specific call characteristics. II. Hyla cinerea (Anura: Hylidae). J Comp Physiol A 161:407–416

    Article  PubMed  CAS  Google Scholar 

  • Mudry KM, Constantine-Paton M, Capranica RR (1977) Auditory sensitivity of the diencephalon of leopard frog Rana p. pipiens. J Comp Physiol A 114:1–13

    Article  Google Scholar 

  • Narins PM (1987) Coding of signals in noise by amphibian auditory nerve fibers. Hear Res 26:145–154

    Article  PubMed  CAS  Google Scholar 

  • Narins PM, Capranica RR (1976) Sexual differences in the auditory system of the tree frog Eleutherodactylus coqui. Science 192:378–380

    Article  PubMed  CAS  Google Scholar 

  • Narins PM, Capranica RR (1980) Neural adaptations for processing the two-note call of the Puerto Rican treefrog, Eleutherodactylus coqui. Brain Behav Evol 17:48–66

    Article  PubMed  CAS  Google Scholar 

  • Narins PM, Wagner I (1989) Noise susceptibility and immunity of phase locking in amphibian auditory-nerve fibers. J Acoust Soc Am 85:1255–1265

    Article  PubMed  CAS  Google Scholar 

  • Nevo E, Capranica RR (1985) Evolutionary origin of ethological reproductive isolation in cricket frogs, Acris. Evol Biol 19:147–214

    Article  Google Scholar 

  • Penna M, Velasquez N, Solis R (2008) Correspondence between evoked vocal responses and auditory thresholds in Pleurodema thaul (Amphibia; Leptodactylidae). J Comp Physiol A 194:361–371

    Article  Google Scholar 

  • Portfors CV, Felix RA (2005) Spectral integration in the inferior colliculus of the CBA/CaJ mouse. Neuroscience 163:1159–1170

    Article  Google Scholar 

  • Richards CL (2006) Has the evolution of complexity in the amphibian papilla influenced anuran speciation rates? J Evol Biol 19:1222–1230

    Article  PubMed  CAS  Google Scholar 

  • Rose G, Capranica RR (1983) Temporal selectivity in the central auditory system of the leopard frog. Science 219:1087–1089

    Article  PubMed  CAS  Google Scholar 

  • Rose GJ, Capranica RR (1984) Processing amplitude-modulated sounds by the auditory midbrain of two species of toads: matched temporal filters. J Comp Physiol A 154:211–219

    Article  Google Scholar 

  • Rose GJ, Capranica RR (1985) Sensitivity to amplitude modulated sounds in the anuran auditory nervous system. J Neurophysiol 53:446–465

    PubMed  CAS  Google Scholar 

  • Rose GJ, Gooler DM (2007) Function of the amphibian central auditory system. In: Narins PM, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer, New York, pp 250–290

    Google Scholar 

  • Rose GJ, Brenowitz EA, Capranica RR (1985) Species specificity and temperature dependency of temporal processing by the auditory midbrain of two species of treefrogs. J Comp Physiol A 157:763–769

    Article  PubMed  CAS  Google Scholar 

  • Rose GJ, Leary CJ, Edwards CJ (2011) Interval-counting neurons in the anuran auditory midbrain: factors underlying diversity of interval tuning. J Comp Physiol A 197:97–108

    Article  Google Scholar 

  • Roth G, Dicke U (1994) Is fixed action pattern a useful concept? In: Greenspan RJ, Kyriacou CP (eds) Flexibility and constraint in behavioral systems. Wiley, New York, pp 3–14

    Google Scholar 

  • Schwartz JJ, Gerhardt HC (1998) The neuroethology of frequency preferences in the spring peeper. Anim Behav 56:55–69

    Article  PubMed  Google Scholar 

  • Schwartz JJ, Simmons AM (1990) Encoding of a spectrally-complex communication sound in the bullfrog’s auditory nerve. J Comp Physiol A 166:489–500

    Article  PubMed  CAS  Google Scholar 

  • Simmons AM, Ferragamo M (1993) Periodicity extraction in the anuran auditory nerve I. “Pitch-shift” effects. J Comp Physiol A 172:57–69

    Article  PubMed  CAS  Google Scholar 

  • Simmons JA, Simmons AM (2011) Bats and frogs and animals in between: evidence for a common central timing mechanism to extract periodicity pitch. J Comp Physiol A 197:585–594

    Article  Google Scholar 

  • Simmons AM, Schwartz JJ, Ferragamo M (1992) Auditory-nerve representation of a complex communication sound in background noise. J Acoust Soc Am 91:2831–2844

    Article  PubMed  CAS  Google Scholar 

  • Simmons AM, Reese G, Ferragamo M (1993) Periodicity extraction in the anuran auditory periphery, II: phase and temporal fine-structure. J Acoust Soc Am 93:3374–3389

    Article  PubMed  CAS  Google Scholar 

  • Simmons AM, Shen Y, Sanderson MI (1996) Neural and computational basis for periodicity extraction in frog peripheral auditory system. Aud Neurosci 2:109–133

    Google Scholar 

  • Simmons AM, Sanderson MI, Garabedian CE (2000) Representation of waveform periodicity in the auditory midbrain of the bullfrog, Rana catesbeiana. J Assoc Res Otolaryngol 1:2–24

    Article  PubMed  CAS  Google Scholar 

  • Simmons AM, Eastman K, Simmons JA (2001) Autocorrelation model of periodicity coding in bullfrog auditory nerve fibers. Acoust Res Lett Online 2:1–6

    Article  Google Scholar 

  • Simmons DD, Meenderink SWF, Vassilakis PN (2007) Anatomy, physiology and function of auditory end organs in the frog inner ear. In: Narins PM, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer, New York, pp 184–220

    Google Scholar 

  • Wells KD, Schwartz JJ (2007) The behavioral ecology of anuran communication. In: Narins PM, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer, New York, pp 44–86

    Google Scholar 

  • Wilczynski W, Endepols H (2007) Central auditory pathways in anuran amphibians: the anatomical basis of hearing and sound communication. In: Narins PM, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer, New York, pp 221–249

    Google Scholar 

  • Wilczynski W, Keddy-Hector AC, Ryan MJ (1992) Call patterns and basilar papilla tuning in cricket frogs. I. Differences among populations and between sexes. Brain Behav Evol 39:229–237

    Article  PubMed  CAS  Google Scholar 

  • Wilczynski W, Rand AS, Ryan MJ (1995) The processing of spectral cues by the call analysis system of the túngara frog, Physalaemus pustulosus. Anim Behav 49:911–929

    Article  Google Scholar 

  • Wilczynski W, Rand AS, Ryan MJ (2001) Evolution of calls and auditory tuning in the Physalaemus pustulosus species group. Brain Behav Evol 58:137–151

    Article  PubMed  CAS  Google Scholar 

  • Yang S, Yang S, Cox CL, Llano DA, Feng AS (2012) Cell’s intrinsic biophysical properties play a role in the systematic decrease in time-locking ability of central auditory neurons. Neuroscience 208:49–57

    Article  PubMed  CAS  Google Scholar 

  • Zelick R, Narins PM (1985) Temporary threshold shift, adaptation, and recovery characteristics of frog auditory nerve fibers. Hear Res 17:161–176

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Bob Capranica was a major influence on my thinking and on my scholarship. Even after his retirement, he continued to inspire me, and by extension my students, by his high standards and his insistence on interpreting physiology in the light of behavior. I thank Jacob Christensen-Dalsgaard, Emma Coddington, Heather Eisthen, Hamilton Farris, and Kim Hoke for organizing the Amphibian Satellite Symposium at ICN2012 and for providing me an opportunity to share my view of Bob’s impact on the field. I was honored to have Bob’s wife, Pat, and his cousin, Tom Capranica, attend my talk. I thank Pat Capranica for sharing the photograph of Bob in Fig. 1. I also thank Mark Bee, Peter M. Narins, James A. Simmons, and an anonymous reviewer for their helpful comments on this manuscript. Research in my laboratory described in this manuscript was supported by National Institute of Health grants NS21911, NS28565 and DC05257.

Author information

Authors and Affiliations

  1. Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, RI, 02912, USA

    Andrea Megela Simmons

Authors
  1. Andrea Megela Simmons
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea Megela Simmons.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Simmons, A.M. “To Ear is Human, to Frogive is Divine”: Bob Capranica’s legacy to auditory neuroethology. J Comp Physiol A 199, 169–182 (2013). https://doi.org/10.1007/s00359-012-0786-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-012-0786-2

Keywords

Search

Navigation