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Bats and frogs and animals in between: evidence for a common central timing mechanism to extract periodicity pitch

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Abstract

Widely divergent vertebrates share a common central temporal mechanism for representing periodicities of acoustic waveform events. In the auditory nerve, periodicities corresponding to frequencies or rates from about 10 Hz to over 1,000 Hz are extracted from pure tones, from low-frequency complex sounds (e.g., 1st harmonic in bullfrog calls), from mid-frequency sounds with low-frequency modulations (e.g., amplitude modulation rates in cat vocalizations), and from time intervals between high-frequency transients (e.g., pulse-echo delay in bat sonar). Time locking of neuronal responses to periodicities from about 50 ms down to 4 ms or less (about 20–300 Hz) is preserved in the auditory midbrain, where responses are dispersed across many neurons with different onset latencies from 4–5 to 20–50 ms. Midbrain latency distributions are wide enough to encompass two or more repetitions of successive acoustic events, so that responses to multiple, successive periods are ongoing simultaneously in different midbrain neurons. These latencies have a previously unnoticed periodic temporal pattern that determines the specific times for the dispersed on-responses.

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Abbreviations

AM:

Amplitude modulation

FM:

Frequency modulation

PRR:

Pulse repetition rate

nVIII:

Auditory nerve

TS:

Torus semicircularis

IC:

Inferior colliculus

VS:

Vector strength

References

  • Bee MA, Bowling AC (2002) Socially-mediated pitch alteration by territorial male bullfrogs, Rana catesbeiana. J Herpetol 36:140–143

    Google Scholar 

  • Brugge JF, Anderson DJ, Hind JE, Rose JE (1969) Time structure of discharges in single auditory nerve fibers of the squirrel monkey in response to complex periodic sounds. J Neurophysiol 32:386–401

    PubMed  CAS  Google Scholar 

  • Brugge JF, Nourski KV, Oya H, Reale RA, Kawasaki H, Steinschneider M, Howard MA III (2009) Coding of repetitive transients by auditory cortex on Heschyl’s gyrus. J Neurophysiol 102:2358–2374

    Article  PubMed  Google Scholar 

  • Cariani PA, Delgutte B (1996) Neural correlates of the pitch of complex tones. I. Pitch and pitch salience. J Neurophysiol 76:1698–1716

    PubMed  CAS  Google Scholar 

  • Cassedy JH, Covey E (1996) A neuroethological theory of the operation of the inferior colliculus. Brain Behav Evol 47:311–336

    Article  Google Scholar 

  • Cedolin L, Delgutte B (2005) Pitch of complex tones: rate-place and interspike interval representations in the auditory nerve. J Neurophysiol 94:347–362

    Article  PubMed  Google Scholar 

  • Dalland J (1965) Hearing sensitivity in bats. Science 150:1185–1186

    Article  PubMed  CAS  Google Scholar 

  • Edamatsu H, Suga N (1993) Differences in response properties of neurons between two delay-tuned areas in the auditory cortex of the mustached bat. J Neurophysiol 69:1700–1712

    PubMed  CAS  Google Scholar 

  • Fay RR (1988) Hearing in vertebrates: a psychophysics databook. Hill-Fay, Winnetka, IL

    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 

  • 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 

  • Haplea S, Covey E, Casseday JH (1994) Frequency tuning and response latencies at three levels in the brainstem of the echolocating bat, Eptesicus fuscus. J Comp Physiol A 174:671–683

    Article  PubMed  CAS  Google Scholar 

  • Heffner RS, Heffner HE (1985) Hearing range of the domestic cat. Hear Res 19:85–88

    Article  PubMed  CAS  Google Scholar 

  • Heffner H, Whitfield IC (1976) Perception of the missing fundamental by cats. J Acoust Soc Am 59:915–919

    Article  PubMed  CAS  Google Scholar 

  • Joris PX, Schreiner CE, Rees A (2004) Neuronal processing of amplitude-modulated sounds. Physiol Rev 84:541–577

    Article  PubMed  CAS  Google Scholar 

  • Kiang NYS, Watanabe T, Thomas T, Clark LF (1965) Discharge patterns of single fibers in the cat’s auditory nerve. MIT Press, Cambridge, MA

    Google Scholar 

  • Koay G, Heffner HE, Heffner RS (1997) Audiogram of the big brown bat (Eptesicus fuscus). Hear Res 105:202–210

    Article  PubMed  CAS  Google Scholar 

  • Langner G (1981) Evidence for neuronal periodicity detection in the auditory system of the guinea fowl: implications for pitch analysis in the time domain. Exp Brain Res 52:333–355

    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 

  • Licklider JCR (1951) A duplex theory of pitch perception. Experientia 7:128–134

    Article  PubMed  CAS  Google Scholar 

  • Liu L-F, Palmer AR, Wallace MN (2006) Phase-locked responses to pure tones in the inferior colliculus. J Neurophysiol 95:1926–1935

    Article  PubMed  Google Scholar 

  • Lu Y, Jen PH-S, Wu M (1998) GABAergic disinhibition affects responses of bat inferior collicular neurons to temporally patterned sound pulses. J Neurophysiol 79:2303–2315

    PubMed  CAS  Google Scholar 

  • Lyon R, Shamma S (1996) Auditory representation of timbre and pitch. In: Hawkins HL, McMullen TA, Popper AN, Fay RR (eds) Auditory computation. Springer, New York, pp 221–270

    Google Scholar 

  • Ma X, Suga N (2008) Corticofugal modulation of the paradoxical latency shifts of inferior collicular neurons. J Neurophysiol 100:1127–1134

    Article  PubMed  Google Scholar 

  • Manley GA, Fastl H, Kössl M, Oeckinhhaus H, Klump G (eds) (2000) Auditory worlds: sensory analysis and perception in animals and man. Wiley-VCH, Weinheim, Germany

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Moore BCJ (2003) An introduction to the psychology of hearing, 5th edn. Academic Press, San Diego

    Google Scholar 

  • Neuweiler G (1990) Auditory adaptations for prey capture in echolocating bats. Physiol Rev 70:615–641

    PubMed  CAS  Google Scholar 

  • Nicastro N (2004) Perceptual and acoustic evidence for species-level differences in meow vocalizations by domestic cats (Felis catus) and African wild cats (Felis silvestris lybica). J Comp Psych 118:287–296

    Article  Google Scholar 

  • Nicastro N, Owren MJ (2003) Classification of domestic cat (Felis catus) vocalizations by native and experienced human listeners. J Comp Psych 117:44–52

    Article  Google Scholar 

  • Pinheiro AD, Wu M, Jen PH (1991) Encoding repetition rate and duration in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Comp Physiol A 169:69–85

    Article  PubMed  CAS  Google Scholar 

  • Poussin C, Simmons JA (1982) Low-frequency hearing sensitivity in the echolocating bat, Eptesicus fuscus. J Acoust Soc Am 72:340–342

    Article  Google Scholar 

  • Rees A, Langner G (2005) Temporal coding in the auditory midbrain. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, New York, pp 346–376

    Chapter  Google Scholar 

  • Reimer K (1987) Coding of sinusoidally amplitude modulated acoustic stimuli in the inferior colliculus of the rufous horseshoe bat, Rhinolophus rouxi. J Comp Physiol A 161:305–313

    Article  PubMed  CAS  Google Scholar 

  • Ritsma RJ (1962) Existence region of the tonal residue. I. J Acoust Soc Am 34:1224–1229

    Article  Google Scholar 

  • Rose JE, Brugge JF, Anderson DJ, Hind JE (1967) Phase-locked response to low-frequency tones in single auditory nerve fibers of the squirrel monkey. J Neurophysiol 30:769–793

    PubMed  CAS  Google Scholar 

  • Sanderson MI, Simmons JA (2000) Neural responses to overlapping FM sounds in the inferior colliculus of echolocating bats. J Neurophysiol 83:1840–1855

    PubMed  CAS  Google Scholar 

  • Sanderson MI, Simmons JA (2005) Target representation of naturalistic echolocation sequences in single unit responses from the inferior colliculus of big brown bats. J Acoust Soc Am 118:3352–3361

    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 

  • Semal C, Demany L (1990) The upper limit of musical pitch. Music Percept 8:165–175

    Google Scholar 

  • Shamma S (2001) On the role of space and time in auditory processing. Trends Cogn Sci 5:340–348

    Article  PubMed  Google Scholar 

  • Simmons JA, Ferragamo MJ, Saliant PA, Haresign T, Wotton JM, Dear SP, Lee DN (1995) Auditory dimensions of acoustic images in echolocation. In: Popper AN, Fay RR (eds) Hearing by bats. Springer, New York, pp 146–190

    Google Scholar 

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

    Google Scholar 

  • Simmons JA, Saillant PA, Ferragamo MJ, Haresign T, Dear SP, Fritz JB, McMullen TA (1996b) Auditory computations for acoustic imaging in bat sonar. In: Hawkins HL, McMullen TA, Popper AN, Fay RR (eds) Auditory computation. Springer, New York, pp 401–468

    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 

  • Stevens KN (1998) Acoustic phonetics. MIT Press, Cambridge, MA

    Google Scholar 

  • Suga N, Olsen JF, Butman JA (1990) Specialized subsystems for processing biologically important complex sounds: cross-correlation analysis for ranging in the bat’s brain. Cold Spring Harbor Symp Quant Biol 55:585–597

    PubMed  CAS  Google Scholar 

  • Suggs DN, Simmons AM (2005) Information theory analysis of patterns of modulation in the advertisement call of the male bullfrog, Rana catesbeiana. J Acoust Soc Am 117:2330–2337

    Article  PubMed  Google Scholar 

  • Walker KMM, Bizley JK, King AJ, Schnupp JWH (2010) Cortical encoding of pitch: recent results and open questions. Hear Res. doi:10.1016/j.heares.2010.04.015

  • Wever EG (1949) Theory of hearing. Wiley, New York

    Google Scholar 

  • Wu CH, Jen PH (2008) Echo frequency selectivity of duration-tuned inferior collicular neurons of the big brown bat, Eptesicus fuscus, determined with pulse-echo pairs. Neuroscience 156:1028–1038

    Article  PubMed  CAS  Google Scholar 

  • Yost WA, Hill R (1978) Strength of the pitches associated with ripple noise. J Acoust Soc Am 64:485–492

    Article  PubMed  CAS  Google Scholar 

  • Young ED, Sachs MB (1979) Representation of steady-state vowels in the temporal aspects of the discharge patterns of populations of auditory-nerve fibers. J Acoust Soc Am 66:1381–1403

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by ONR Grant # N00014-04-l-0415, by NIH Grant # R01-MH069633, and by NSF Grant # IOS-0843522 (JAS), and by NIH grant DC05257 (AMS). We thank the members of the Brown bat and frog labs for discussion of this work.

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Authors and Affiliations

  1. Department of Neuroscience, Brown University, Box GLN, Providence, RI, 02912, USA

    James A. Simmons & Andrea Megela Simmons

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

    Andrea Megela Simmons

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  1. James A. Simmons
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Correspondence to James A. Simmons.

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Simmons, J.A., Megela Simmons, A. 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 (2011). https://doi.org/10.1007/s00359-010-0607-4

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