Skip to main content
Log in

Duration tuning in the auditory midbrain of echolocating and non-echolocating vertebrates

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

Abstract

Neurons tuned for stimulus duration were first discovered in the auditory midbrain of frogs. Duration-tuned neurons (DTNs) have since been reported from the central auditory system of both echolocating and non-echolocating mammals, and from the central visual system of cats. We hypothesize that the functional significance of auditory duration tuning likely varies between species with different evolutionary histories, sensory ecologies, and bioacoustic constraints. For example, in non-echolocating animals such as frogs and mice the temporal filtering properties of auditory DTNs may function to discriminate species-specific communication sounds. In echolocating bats duration tuning may also be used to create cells with highly selective responses for specific rates of frequency modulation and/or pulse-echo delays. The ability to echolocate appears to have selected for high temporal acuity in the duration tuning curves of inferior colliculus neurons in bats. Our understanding of the neural mechanisms underlying sound duration selectivity has improved substantially since DTNs were first discovered almost 50 years ago, but additional research is required for a comprehensive understanding of the functional role and the behavioral significance that duration tuning plays in sensory systems.

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

Access this article

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

Similar content being viewed by others

Abbreviations

AC:

Auditory cortex

CF:

Constant frequency

CNS:

Central nervous system

DTN:

Duration-tuned neuron

FM:

Frequency modulation

IC:

Inferior colliculus

MGB:

Medial geniculate body

OFFE :

Offset-evoked excitation

ONE :

Onset-evoked excitation

PT:

Pure tone

SPL:

Sound pressure level

SUSI :

Sustained onset-evoked inhibition

TS:

Torus semicircularis

References

  • Au WWL (2000) Echolocation in dolphins. In: Au WWL, Popper AN, Fay RR (eds) Hearing by whales and dolphins. Springer, New York, pp 364–408

    Google Scholar 

  • Aubie B, Becker S, Faure PA (2009) Computational models of millisecond level duration tuning in neural circuits. J Neurosci 29:9255–9270

    PubMed  CAS  Google Scholar 

  • Brand A, Urban A, Grothe B (2000) Duration tuning in the mouse auditory midbrain. J Neurophysiol 84:1790–1799

    PubMed  CAS  Google Scholar 

  • Brown KA, Buchwald JS, Johnson JR, Mikolich DJ (1978) Vocalization in the cat and kitten. Dev Psychobiol 11:559–570

    PubMed  CAS  Google Scholar 

  • Capranica RR (1968) The vocal repertoire of the bullfrog (Rana catesbeiana). Behaviour 31:302–325

    Google Scholar 

  • Carlson BA (2009) Temporal-pattern recognition by single neurons in a sensory pathway devoted to social communication behavior. J Neurosci 29:9417–9428

    PubMed  CAS  Google Scholar 

  • Carr CE, Konishi M (1990) A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10:3227–3246

    PubMed  CAS  Google Scholar 

  • Casseday JH, Ehrlich D, Covey E (1994) Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. Science 264:847–850

    PubMed  CAS  Google Scholar 

  • Casseday JH, Ehrlich D, Covey E (2000) Neural measurement of sound duration: control by excitatory–inhibitory interactions in the inferior colliculus. J Neurophysiol 84:1475–1487

    PubMed  CAS  Google Scholar 

  • Chen GD (1998) Effects of stimulus duration on responses of neurons in the chinchilla inferior colliculus. Hear Res 112:142–150

    Google Scholar 

  • Covey E, Casseday JH (1991) The monaural nuclei of the lateral lemniscus in an echolocating bat: parallel pathways for analyzing temporal features of sound. J Neurosci 11:3456–3470

    PubMed  CAS  Google Scholar 

  • Covey E, Faure PA (2005) Neural mechanisms for analyzing temporal patterns in echolocating bats. In: Pressnitzer D, de Cheveigné A, McAdams S, Collet L (eds) Auditory signal processing: physiology, psychoacoustics, and models. Springer, New York, pp 251–257

    Google Scholar 

  • Covey E, Kauer JA, Casseday JH (1996) Whole-cell patch-clamp recording reveals subthreshold sound-evoked postsynaptic currents in the inferior colliculus of awake bats. J Neurosci 16:3009–3018

    PubMed  CAS  Google Scholar 

  • Dear SP, Suga N (1995) Delay-tuned neurons in the midbrain of the big brown bat. J Neurophys 73:1084–1100

    CAS  Google Scholar 

  • Dear SP, Simmons JA, Fritz J (1993) A possible neuronal basis for representation of acoustic scenes in the auditory cortex of the big brown bat. Nature 364:620–623

    PubMed  CAS  Google Scholar 

  • Duysens J, Schaafsma SJ, Orban GA (1996) Cortical off response tuning for stimulus duration. Vision Res 36:3243–3251

    PubMed  CAS  Google Scholar 

  • Edwards CJ, Alder TB, Rose GJ (2002) Auditory midbrain neurons that count. Nat Neurosci 5:934–936

    PubMed  CAS  Google Scholar 

  • Ehrlich D, Casseday JH, Covey E (1997) Neural tuning to sound duration in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Neurophysiol 77:2360–2372

    PubMed  CAS  Google Scholar 

  • Faure PA, Barclay RMR (1994) Substrate-gleaning versus aerial-hawking: plasticity in the foraging and echolocation behaviour of the long-eared bat, Myotis evotis. J Comp Physiol A 174:651–660

    PubMed  CAS  Google Scholar 

  • Faure PA, Fremouw T, Casseday JH, Covey E (2003) Temporal masking reveals properties of sound-evoked inhibition in duration-tuned neurons of the inferior colliculus. J Neurosci 23:3052–3065

    PubMed  CAS  Google Scholar 

  • Fremouw T, Faure PA, Casseday JH, Covey E (2005) Duration selectivity of neurons in the inferior colliculus of the big brown bat: tolerance to changes in sound level. J Neurophysiol 94:1869–1878

    PubMed  Google Scholar 

  • Fuzessery ZM, Hall JC (1999) Sound duration selectivity in the pallid bat inferior colliculus. Hear Res 137:137–154

    PubMed  CAS  Google Scholar 

  • Fuzessery ZM, Buttenhoff P, Andrews B, Kennedy JM (1993) Passive sound localization of prey by the pallid bat (Antrozous p. pallidus). J Comp Physiol A 171:767–777

    PubMed  CAS  Google Scholar 

  • Fuzessery ZM, Richardson MD, Coburn MS (2006) Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the inferior colliculus of the pallid bat. J Neurophysiol 96:1320–1336

    PubMed  Google Scholar 

  • Galazyuk AV, Feng AS (1997) Encoding of sound duration by neurons in the auditory cortex of the little brown bat, Myotis lucifugus. J Comp Physiol A 180:301–311

    PubMed  CAS  Google Scholar 

  • Gittelman JX, Li N, Pollak GD (2009) Mechanisms underlying directional selectivity for frequency-modulated sweeps in the inferior collculus revealed by in vivo whole-cell recordings. J Neurosci 29:13030–13041

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Griffin DR, Webster FA, Michael CR (1960) The echolocation of flying insects by bats. Anim Behav 8:141–154

    Google Scholar 

  • Grothe B, Park TJ, Schuller G (1997) Medial superior olive in the free-tailed bat: response to pure tones and amplitude-modulated tones. J Neurophysiol 77:1553–1565

    PubMed  CAS  Google Scholar 

  • Grothe B, Covey E, Casseday JH (2001) Medial superior olive of the big brown bat: neuronal responses to pure tones, amplitude modulations, and pulse trains. J Neurophysiol 86:2219–2230

    PubMed  CAS  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 Phys A 174:671–683

    CAS  Google Scholar 

  • He J (2002) OFF responses in the auditory thalamus of the guinea pig. J Neurophysiol 88:2377–2386

    PubMed  Google Scholar 

  • He J, Hashikawa T, Ojima H, Kinouchi Y (1997) Temporal integration and duration tuning in the dorsal zone of cat auditory cortex. J Neurosci 17:2615–2625

    PubMed  CAS  Google Scholar 

  • Hooper SL, Buchman E, Hobbs KH (2002) A computational role for slow conductances: single-neuron models that measure duration. Nat Neurosci 5:552–556

    PubMed  CAS  Google Scholar 

  • Hunyady H (2008) Vocal sounds of the chinchilla. MS Thesis, Bowling Green State University, Ohio

  • Jen PHS, Feng RB (1999) Bicuculline application affects discharge pattern and pulse-duration tuning characteristics of bat inferior collicular neurons. J Comp Physiol A 184:185–194

    PubMed  CAS  Google Scholar 

  • Jen PHS, Wu CH (2005) The role of GABAergic inhibition in shaping the response size and duration selectivity of bat inferior collicular neurons to sound pulses in rapid sequences. Hear Res 202:222–234

    PubMed  CAS  Google Scholar 

  • Jen PHS, Wu CH (2006) Duration selectivity organization in the inferior colliculus of the big brown bat, Eptesicus fuscus. Brain Res 1108:76–87

    PubMed  CAS  Google Scholar 

  • Jen PHS, Zhou XM (1999) Temporally patterned pulse trains affect duration tuning characteristics of bat inferior collicular neurons. J Comp Physiol A 185:471–478

    PubMed  CAS  Google Scholar 

  • Jones G, Teeling EC (2006) The evolution of echolocation in bats. Trends Ecol Evol 21:149–156

    PubMed  Google Scholar 

  • Kalko EKV, Schnitzler HU (1989) The echolocation and hunting behavior of Daubenton’s bat, Myotis daubentoni. Behav Ecol Sociobiol 24:225–238

    Google Scholar 

  • Kiang NYS (1965) Discharge patterns of single fibers in the cat’s auditory nerve. MIT Press, Cambridge

    Google Scholar 

  • Knudsen EI, Konishi M (1979) Mechanisms of sound localization in the barn owl (Tyto alba). J Comp Physiol A 133:13–21

    Google Scholar 

  • Knutson B, Burgdorf J, Panksepp J (2002) Ultrasonic vocalizations as indices of affective states in rats. Psych Bull 128:961–977

    Google Scholar 

  • Koch U, Grothe B (2003) Hyperpolarization-activated current (Ih) in the inferior colliculus: distribution and contribution to temporal processing. J Neurophysiol 90:3679–3687

    PubMed  Google Scholar 

  • Kössl M, Mora E, Coro F, Vater M (1999) Two-toned echolocation calls from Molossus molossus in Cuba. J Mammal 80:929–932

    Google Scholar 

  • Kuwada S, Batra R, Yin TCT, Oliver DL, Haberly LB, Stanford TR (1997) Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat. J Neurosci 17:7565–7581

    PubMed  CAS  Google Scholar 

  • Large EW, Crawford JD (2002) Auditory temporal computation: interval selectivity based on post-inhibitory rebound. J Comp Neurosci 13:125–142

    Google Scholar 

  • Le Beau FE, Rees A, Malmierca MS (1996) Contribution of GABA- and glycine-mediated inhibition to the monaural temporal response properties of neurons in the inferior colliculus. J Neurophysiol 75:902–919

    PubMed  CAS  Google Scholar 

  • Leary CJ, Edwards CJ, Rose GJ (2008) Midbrain auditory neurons integrate excitation and inhibition to generate duration selectivity: an in vivo whole-cell patch study in anurans. J Neurosci 28:5481–5493

    PubMed  CAS  Google Scholar 

  • Li N, Gittelman JX, Pollak GD (2010) Intracellular recordings reveal novel features of neurons that code interaural intensity disparities in the inferior colliculus. J Neurosci 30:14573–14584

    PubMed  CAS  Google Scholar 

  • Liu RC, Miller KD, Merzenich MM, Schreiner CE (2003) Acoustic variability and distinguishability among mouse ultrasound vocalizations. J Acoust Soc Am 114:3412–3422

    PubMed  Google Scholar 

  • Luo F, Metzner W, Wu FJ, Zhang SY, Chen QC (2008) Duration-sensitive neurons in the inferior colliculus of horseshoe bats: adaptations for using CF-FM echolocation pulses. J Neurophysiol 99:284–296

    PubMed  Google Scholar 

  • Ma CL, Kelly JB, Wu SH (2002) AMPA and NMDA receptors mediate synaptic excitation in the rat’s inferior colliculus. Hear Res 168:25–34

    PubMed  CAS  Google Scholar 

  • Mecham J (1971) Vocalizations of the leopard frog, Rana pipiens, and three related Mexican species. Copeia 1971:505–516

    Google Scholar 

  • Melendez KV, Jones DL, Feng AS (2006) Classification of communication signals of the little brown bat. J Acoust Soc Am 120:1095–1102

    PubMed  Google Scholar 

  • Mora EC, Kössl M (2004) Ambiguities in sound-duration selectivity by neurons in the inferior colliculus of the bat Molossus molossus from Cuba. J Neurophysiol 91:2215–2226

    PubMed  Google Scholar 

  • Mörchen A, Rheinlaender J, Schwartzkopff J (1978) Latency shift in insect auditory nerve fibers. Naturwissenschaften 65:656–657

    Google Scholar 

  • Moss CF, Surlykke A (2001) Auditory scene analysis by echolocation in bats. J Acoust Soc Am 110:2207–2226

    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

    PubMed  CAS  Google Scholar 

  • Nelson PG, Erulkar SD (1963) Synaptic mechanisms of excitation and inhibition in the central auditory pathway. J Neurophysiol 26:908–923

    PubMed  CAS  Google Scholar 

  • Neuweiler G (1984) Foraging, echolocation and audition in bats. Naturwissenschaften 71:446–455

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • O’Neill WE, Suga N (1979) Target range-sensitive neurons in the auditory cortex of the mustache bat. Science 203:69–73

    PubMed  Google Scholar 

  • Olsen JF, Suga N (1991) Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of target range information. J Neurophysiol 65:1275–1296

    PubMed  CAS  Google Scholar 

  • Pedemonte M, Torterolo P, Velluti RA (1997) In vivo intracellular characteristics of inferior colliculus neurons in guinea pigs. Brain Res 759:24–31

    PubMed  CAS  Google Scholar 

  • Pérez-González D, Malmierca MS, Moore JM, Hernández O, Covey E (2006) Duration selective neurons in the inferior colliculus of the rat: topographic distribution and relation of duration sensitivity to other response properties. J Neurophysiol 95:823–836

    PubMed  Google Scholar 

  • Peterson DC, Voytenko S, Gans D, Galazyuk A, Wenstrup J (2008) Intracellular recordings from combination-sensitive neurons in the inferior colliculus. J Neurophysiol 100:629–645

    PubMed  Google Scholar 

  • Petrites AE, Eng OS, Mowlds DS, Simmons JA, DeLong CM (2009) Interpulse interval modulation by echolocating big brown bats (Eptesicus fuscus) in different densities of obstacle clutter. J Comp Physiol A 195:603–617

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Pollack GS, Hoy RR (1979) Temporal pattern as a cue for species-specific calling song recognition in crickets. Science 204:429–432

    PubMed  CAS  Google Scholar 

  • Potter HD (1965) Patterns of acoustically evoked discharges of neurons in the mesencephalon of the bullfrog. J Neurophysiol 28:1155–1184

    PubMed  CAS  Google Scholar 

  • Razak KA, Fuzessery ZM (2006) Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the auditory cortex of the pallid bat. J Neurophysiol 96:1320–1336

    Google Scholar 

  • Rose JE, Greenwood DD, Goldberg JM, Hind JE (1963) Some discharge characteristics of single neurons in the inferior colliculus of the cat. I. Tonotopical organization, relation of spike-counts to tone intensity, and firing patterns of single elements. J Neurophysiol 26:294–320

    Google Scholar 

  • Sanchez JT, Gans D, Wenstrup JJ (2007) Contribution of NMDA and AMPA receptors to temporal patterning of auditory responses in the inferior colliculus. J Neurosci 27:1954–1963

    PubMed  CAS  Google Scholar 

  • Seidl AH, Rubel EW, Harris DM (2010) Mechanisms for adjusting interaural time differences to achieve binaural coincidence detection. J Neurosci 30:70–80

    PubMed  CAS  Google Scholar 

  • Shannon RV, Zeng FG, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primarily temporal cues. Science 270:303–304

    PubMed  CAS  Google Scholar 

  • Simmons JA (1973) The resolution of target range by echolocating bats. J Acoust Soc Am 54:157–173

    PubMed  CAS  Google Scholar 

  • Simmons JA (1989) A view of the world through the bat’s ear: the formation of acoustic images in echolocation. Cognition 33:155–199

    PubMed  CAS  Google Scholar 

  • Simmons JA, Stein RA (1980) Acoustic imaging in bat sonar: echolocation signals and the evolution of echolocation. J Comp Physiol A 135:61–84

    Google Scholar 

  • Singh S, Mountain DC (1997) A model for duration coding in the inferior colliculus. In: Bower JM (ed) Computational neuroscience: trends in research. Plenum Press, New York, pp 497–503

    Google Scholar 

  • Sivaramakrishnan S, Oliver DL (2001) Distinct K currents result in physiologically distinct cell types in the inferior colliculus of the rat. J Neurosci 21:2861–2877

    PubMed  CAS  Google Scholar 

  • Suga N, Horikawa J (1986) Multiple time axes for representation of echos in the auditory cortex of the mustached bat. J Neurophysiol 55:776–805

    PubMed  CAS  Google Scholar 

  • Sun H, Wu SH (2008) Physiological characteristics of postinhibitory rebound depolarization in neurons of the rat’s dorsal cortex of the inferior colliculus studied in vitro. Brain Res 1226:70–81

    PubMed  CAS  Google Scholar 

  • Surlykke A, Moss CF (2000) Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory. J Acoust Soc Am 110:2419–2429

    Google Scholar 

  • Sutter ML (2000) Shapes and level tolerances of frequency tuning curves in primary auditory cortex: quantitative measures and population codes. J Neurophysiol 84:1012–1025

    PubMed  CAS  Google Scholar 

  • Tanaka H, Wong D, Taniguchi I (1992) The influence of stimulus duration on the delay tuning of cortical neurons in the FM bat, Myotis lucifugus. J Comp Physiol A 171:29–40

    PubMed  CAS  Google Scholar 

  • Thomas JA, Moss CF, Vater M (eds) (2004) Echolocation in bats and dolphins. The University of Chicago Press, Chicago

    Google Scholar 

  • Vater M, Covey E, Casseday JH (1997) The columnar region of the ventral nucleus of the lateral lemniscus in the big brown bat (Eptesicus fuscus): synaptic arrangements and structural correlates of feedforward inhibitory function. Cell Tissue Res 289:223–233

    PubMed  CAS  Google Scholar 

  • Veselka N, McErlain DD, Holdsworth DW, Eger JL, Chhem RK, Mason MJ, Brain KL, Faure PA, Fenton MB (2010) A bony connection signals laryngeal echolocation in bats. Nature 463:939–942

    PubMed  CAS  Google Scholar 

  • Voytenko SV, Galazyuk AV (2007) Intracellular recording reveals temporal integration in inferior colliculus neurons of awake bats. J Neurophysiol 97:1368–1378

    PubMed  CAS  Google Scholar 

  • Voytenko SV, Galazyuk AV (2008) Timing of sound-evoked potentials and spike responses in the inferior colliculus of awake bats. Neuroscience 155:923–936

    PubMed  CAS  Google Scholar 

  • Wang J, van Wijhe R, Chen Z, Yin S (2006) Is duration tuning a transient process in the inferior colliculus of guinea pigs? Brain Res 1114:63–74

    PubMed  CAS  Google Scholar 

  • Wang X, Luo F, Wu FJ, Chen QC, Jen PHS (2008) The recovery cycle of bat duration-selective collicular neurons varies with hunting phase. Neuroreport 19:861–865

    PubMed  Google Scholar 

  • Wang X, Luo F, Jen PHS, Chen QC (2010) Recovery cycle of neurons in the inferior colliculus of the FM bat determined with varied pulse-echo duration and amplitude. Chin J Physiol 53:119–129

    PubMed  Google Scholar 

  • Winer JA, Schreiner CE (eds) (2005) The inferior colliculus. Springer, New York

    Google Scholar 

  • Wu CH, Jen PHS (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

    PubMed  CAS  Google Scholar 

  • Xia YF, Qi ZH, Shen JX (2000) Neural representation of sound duration in the inferior colliculus of the mouse. Acta Otolaryngol 120:638–643

    PubMed  CAS  Google Scholar 

  • Xie R, Gittelman JX, Pollak GD (2007) Rethinking tuning: in vivo whole-cell recordings of the inferior colliculus in awake bats. J Neurosci 27:9469–9481

    PubMed  CAS  Google Scholar 

  • Xie R, Gittelman JX, Li N, Pollak GD (2008) Whole cell recordings of intrinsic properties and sound-evoked responses from the inferior colliculus. Neuroscience 154:245–256

    PubMed  CAS  Google Scholar 

  • Yin S, Chen Z, Yu D, Feng Y, Wang J (2008) Local inhibition shapes duration tuning in the inferior colliculus of guinea pigs. Hear Res 237:32–48

    PubMed  Google Scholar 

  • Zhou X, Jen PHS (2001) The effect of sound intensity on duration-tuning characteristics of bat inferior collicular neurons. J Comp Physiol A 187:63–73

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Gerhard Neuweiler had a profound influence on the field of bat echolocation as evidenced both by the quality of research and outstanding scientists stemming from his laboratory. PAF wishes he had met Professor Neuweiler. Research supported by a Discovery Grant (PAF) and a Canada Graduate Scholarship (BA) from the Natural Sciences and Engineering Research Council (NSERC) of Canada. The McMaster Bat Lab is also supported by infrastructure grants from the Canada Foundation for Innovation and the Ontario Innovation Trust. Research approved by the McMaster University Animal Research Ethics Board, and in accordance with the Canadian Council on Animal Care.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul A. Faure.

Additional information

R. Sayegh and B. Aubie contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sayegh, R., Aubie, B. & Faure, P.A. Duration tuning in the auditory midbrain of echolocating and non-echolocating vertebrates. J Comp Physiol A 197, 571–583 (2011). https://doi.org/10.1007/s00359-011-0627-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-011-0627-8

Keywords

Navigation