Skip to main content
SpringerLink
Log in

Neurons with different temporal firing patterns in the inferior colliculus of the little brown bat differentially process sinusoidal amplitude-modulated signals

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

Abstract

We examined how well single neurons in the inferior colliculus (IC) of an FM bat (Myotis lucifugus) processed simple tone bursts of different duration and sinusoidal amplitude-modulated (SAM) signals that approximated passively heard natural sounds. Units' responses to SAM tones, measured in terms of average spike count and firing synchrony to the modulation envelope, were plotted as a function of the modulation frequency to construct their modulation transfer functions. These functions were classified according to their shape (e.g., band-, low-, high-, and all-pass). IC neurons having different temporal firing patterns to simple tone bursts (tonic, chopper, onset-late, and onset-immediate) exhibited different selectivities for SAM signals. All tonic and 83% of chopper neurons responded robustly to SAM signals and displayed a variety of spike count-based response functions. These neurons showed a decreased level of time-locking as the modulation frequency was increased, and thereby gave low-pass synchronization-based response functions. In contrast, 64% of onset-immediate, 37% of onset-late and 17% of chopper units failed to respond to SAM signals at any modulation frequency tested (5–800 Hz). Those onset neurons that did respond to SAM showed poor time-locking (i.e., non-significant levels of synchronization). We obtained evidence that the poor SAM response of some onset and chopper neurons was due to a preference for short-duration signals. These data suggest that tonic and most chopper neurons are better-suited for the processing of long-duration SAM signals related to passive hearing, whereas onset neurons are better-suited for the processing of short, pulsatile signals such as those used in echolocation.

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

Similar content being viewed by others

Abbreviations

C:

chopper

FM:

frequency-modulated

IC:

inferior colliculus

MTF:

modulation transfer function

O1 :

onset-immediate

OL :

onset-late

PAM:

pulsatile amplitude-modulation

PSTH:

peri-stimulus time histogram

SAM:

sinusoidal amplitude-modulation

SC:

synchronization coefficient

T:

tonic

References

  • Anderson ME, Racey PA (1993) Discrimination between fluttering and non-fluttering moths by brown long-eared bats, Plecotus aritus. Anim Behav 46: 1151–1155

    Google Scholar 

  • Barclay RMR, Thomas DW (1979) Copulation call of Myotis lucifugus: A discrete situation specific communication signal. J Mammal 60: 632–634

    Google Scholar 

  • Barclay RMR, Fenton MB, Thomas DW (1979) Social behavior of the little brown bat, Myotis lucifugus. II. Vocal communication. Behav Ecol Sociobiol 6: 137–146

    Google Scholar 

  • Batra R, Shigeyuki K, Stanford TR (1989) Temporal coding of envelopes and their interaural delays in the inferior colliculus of the unanesthetized rabbit. J Neurophysiol 61: 257–268

    Google Scholar 

  • Bell GP, Fenton MB (1984) The use of Doppler-shifted echoes as flutter detection and clutter rejection system: The echolocation and feeding behavior of Hipposideros ruber (Chiroptera: Hipposideridae). Behav Ecol Sociobiol 15: 109–114

    Google Scholar 

  • Bodenhamer RD, Pollak GD (1981) Time and frequency domain processing in the inferior colliculus of echolocating bats. Hearing Res 5: 317–335

    Google Scholar 

  • Bodenhamer RD, Pollak GD, Marsh DS (1979) Coding of the fine frequency information by echo ranging neurons in the inferior colliculus of the Mexican free-tailed bat. Brain Res 171: 530–535

    Google Scholar 

  • Buchler ER, Childs SB (1981) Orientation to distant sounds by foraging big brown bats (Eptesicus fuscus). Anim Behav 29: 428–432

    Google Scholar 

  • Buunen TJF, Rhode WS (1978) Responses of fibers in the cat's auditory nerve to the cubic difference tone. J Acoust Soc Am 64: 772–781

    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

    Google Scholar 

  • Condon CJ (1994) Processing of amplitude-modulated acoustic signals in the auditory system of the little brown bat, Myotis lucifugus: implications for the recognition of insect prey. PhD Thesis, Neuroscience. University of Illinois, Urbana-Champaign

    Google Scholar 

  • Condon CJ, Chang S-H, Feng AS (1991) Processing of behaviorally relevant temporal parameters of acoustic stimuli by single neurons in the superior olivary nucleus of the leopard frog. J Comp Physiol A 168: 709–725

    Google Scholar 

  • Condon CJ, White KR, Feng AS (1993) Neurons in the inferior colliculus and auditory cortex of the little brown bat selectively process amplitude-modulated signals that mimic echoes from fluttering insect targets. Soc Neurosci Abstr 19: 739

    Google Scholar 

  • Condon CJ, White KR, Feng AS (1994) Processing of amplitudemodulated signals that mimic echoes from fluttering targets in the inferior colliculus of the little brown bat, Myotis lucifugus. J Neurophysiol 71: 768–784

    Google Scholar 

  • Condon CJ, Chang S-H, Feng AS (1995) Classification of the temporal firing patterns of single units in the frog superior olivary nucleus. Hearing Res 83: 190–202

    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

    Google Scholar 

  • Emde G von der, Menne D (1989) Discrimination of insect wing beat-frequencies by the bat Rhinolophus ferrumequinum. J Comp Physiol A 164: 663–671

    Google Scholar 

  • Eggermont JJ (1990) Temporal modulation transfer functions for single neurons in the auditory midbrain of the leopard frog. Intensity and carrier-frequency dependence. Hearing Res 43: 181–198

    Google Scholar 

  • Faure PA, Barclay RMR (1994) Substrate-gleaning versus aerialhawking: plasticity in the foraging and echolocation behaviour of the long-eared bat, Myotis evotis. 3 Comp Physiol A 174: 651–660

    Google Scholar 

  • Feng AS, Simmons JA, Kick SA (1978) Echo detection and targetranging neurons in the auditory system of the bat Eptesicus fuscus. Science 202: 645–648

    Google Scholar 

  • Feng AS, Simmons JA, Kick SA, Lawrence BD (1980) Neural mechanisms for target ranging in an echolocating bat Eptesicus fuscus. In: Bushnell RG, Fish JF (eds) Animal Sonar Systems. Plenum Publishing, New York, pp 885–887

    Google Scholar 

  • Feng AS, Condon CJ, White KR (1994) Stroboscopic hearing as a mechanism for prey discrimination in FM bats? J Acoust Soc Am 95: 2736–2744

    Google Scholar 

  • Fenton MB (1980) Adaptiveness and ecology of echolocation in terrestrial (aerial) systems. In: Bushnell RG, Fish JF (eds) Animal Sonar Systems. Plenum Press, New York, pp 427–446

    Google Scholar 

  • Fenton MB, Bell GP (1979) Echolocation and feeding behavior in four species of Myotis (Chiroptera). Can J Zool 57: 1271–1277

    Google Scholar 

  • Fuzessery ZM (1994) Response selectivity for multiple dimensions of frequency sweeps in the pallid bat inferior colliculus. J Neurophysiol 72: 1061–1079

    Google Scholar 

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

    Google Scholar 

  • Goldberg, JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: Some physiological mechanisms of sound localization. J Neurophysiol 32: 613–636

    CAS  PubMed  Google Scholar 

  • Goldman LJ, Henson OW (1977) Prey recognition and selection by the constant frequency bat, Pteronotus p. parnelli. Behav Ecol Sociobiol 2: 411–419

    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

    Google Scholar 

  • Gould E (1971) Studies of maternal-infant communication and development of vocalizations in the bats Myotis and Eptesicus. Comm Behav Biol 5: 263–313

    Google Scholar 

  • Griffin DR (1958) Listening in the Dark. Yale University Press, New Haven, CT

    Google Scholar 

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

    Google Scholar 

  • Hall JC, Feng AS (1988) Influence of envelope rise time on neural responses in the auditory system of anurans. Hearing Res 36: 261–276

    Google Scholar 

  • Hamr J, Bailey ED (1985) Detection and discrimination of insect flight sounds by big brown bats (Eptesicusfuscus). Biol Behav 10: 105–121

    Google Scholar 

  • Jen PH-S, Schlegel PA (1982) Auditory physiological properties of neurones in the inferior colliculus of the big brown bat, Eptesicus fuscus. Comp Physiol 147: 351–362

    Google Scholar 

  • Kanwal JS, Matsumura S, Ohlemiller K, Suga N (1994) Analysis of acoustic elements and syntax in communication sounds emitted by mustached bats. J Acoust Soc Am 96: 1229–1254

    Google Scholar 

  • Kober R, Schnitzler HU (1990) Information in sonar echoes of fluttering insects available for echolocating bats. J Acoust Soc Am 87: 882–896

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Lesser HD, O'Neill WE, Frisina RD, Emerson RC (1990) On-off units in the mustached bat inferior colliculus are selective for transients resembling “acoustic glint” from fluttering insect targets. Exp Brain Res 82: 137–148

    Google Scholar 

  • Link A, Marimuthu G, Neuweiler G (1986) Movement as a specific stimulus for prey catching behavior in rhinolophid and hipposiderid bats. J Comp Physiol A 159: 403–403–413

    Google Scholar 

  • Miller LA, Degn HJ (1981) The acoustic behavior of four species of Vespertilionid bats studied in the field. J Comp Physiol 142: 67–74

    Google Scholar 

  • Møller AR (1969) Unit responses in the rat cochlear nucleus to repetitive transient sounds. Acta Physiol Scand 75: 542–551

    Google Scholar 

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

    Google Scholar 

  • O'Neill WE (1985) Responses to pure tones and linear FM components of the CF-FM biosonar signal by single units in the inferior colliculus of the mustached bat. J Comp Physiol A 157: 797–815

    Google Scholar 

  • Pfeiffer RR (1966) Classification of response patterns of spike discharges for units in the cochlear nucleus: tone burst stimulation. Exp Brain Res 1: 220–235

    Google Scholar 

  • Phillips DP, Hall SE (1990) Response timing constraints on the cortical representation of sound time structure. J Acoust Soc Am 88: 1403–1411

    Google Scholar 

  • Phillips DP, Semple MN, Kitzes LM (1995) Factors shaping the tone level sensitivity of single neurons in posterior field of cat auditory cortex. J Neurophysiol 73: 674–686

    Google Scholar 

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

    Google Scholar 

  • Pollak GD, Marsh DS, Bodenhamer R, Souther A (1977) Characteristics of phasic on neurons in inferior colliculus of unanesthetized bats with observations relating to mechanisms for echo ranging. J Neurophysiol 40: 926–942

    Google Scholar 

  • Reimer K (1987) Coding of sinusoidally amplitude modulated acoustic stimuli in the inferior colliculus of the rufous horseshoe bat, Rhinolophus rouxi. 3 Comp Physiol A 161: 305–313

    Google Scholar 

  • Rees A, Møller AR (1983) Responses of neurons in the inferior colliculus of the rat to AM and FM tones. Hearing Res 10: 301–330

    Google Scholar 

  • Rees A, Palmer AR (1989) Neuronal responses to amplitudemodulated and pure-tone stimuli in the guinea pig inferior colliculus, and their modification by broad-band noise. J Acoust Soc Am 85: 1978–1994

    Google Scholar 

  • Ryan MJ, Tuttle MD (1987) The role of prey-generated sounds, vision, and echolocation in prey localization by the African bat Cardioderma cor (Megadermatidae). J Comp Physiol A 161: 59–66

    Google Scholar 

  • Schnitzler H-U (1987) Echoes of fluttering insects: information for echolocating bats. In: Fenton MB, Racey P, Rayner JMV (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge, pp 226–243

    Google Scholar 

  • Schnitzler H-U, Flieger E (1983) Detection of oscillating target movements by echolocation in the greater horseshoe bat. J Comp Physiol 153: 385–391

    Google Scholar 

  • Schnitzler H-U, Henson OW (1980) Performance of airborne animal sonar systems. I. Microchiroptera. In: Busnel RG, Fish JF (eds) Animal Sonar Systems, Plenum Press, New York pp 109–181

    Google Scholar 

  • Schnitzler H-U, Menne D, Kober R, Heblich K (1983) The acoustical image of fluttering insects in echolocating bats. In: Huber F, Markl H (eds) Neuroethology and behavioral physiology, Springer Berlin and Heidelberg, pp 235–250

    Google Scholar 

  • Schuller G (1979) Coding of small sinusoidal frequency and amplitude modulations in the inferior colliculus of “CF-FM” bat, Rhinolophus ferrumequinum. Exp Brain Res 34: 117–132

    Google Scholar 

  • Schuller G (1984) Natural ultrasonic echoes from wing beating insects are encoded by collicular neurons in the CF-FM bat, Rhinolophus ferrumequinum. J Comp Physiol A 155: 121–128

    Google Scholar 

  • Simmons JA (1971) Echolocation in bats: signal processing of echoes for target range. Science 171: 925–928

    Google Scholar 

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

    Google Scholar 

  • Sotavalta O (1947) The flight tone (wing-stroke frequency) of insects. Acta Entomol Fennica 4–5: 5–115

    Google Scholar 

  • Suga N (1969) Classification of inferior collicular neurons of bats in terms of responses to pure tones, FM sounds, and noise bursts. J Physiol (Lond) 200: 555–574

    Google Scholar 

  • Suga N (1970) Echo-ranging neurons in the inferior colliculus of bats. Science 170: 449–452

    Google Scholar 

  • Suga N (1971) Responses of inferior collicular neurons of bats to tone bursts with different rise times. J Physiol (London) 217: 159–177

    Google Scholar 

  • Thomas DW, Fenton MB, Barclay RMR (1979) Social behavior of the little brown bat, Myotis lucifugus I. Mating behavior. Behav Ecol Sociobiol 6: 129–136

    Google Scholar 

  • Treat AE (1955) The response to sound in certain Lepidoptera. Ann Entomol Soc Am 48: 272–284

    Google Scholar 

  • Vater M (1982) Single unit responses in cochlear nucleus of horseshoe bats to sinusoidal frequency and amplitude modulated signals. J Comp Physiol 149: 369–388

    Google Scholar 

Download references

Author information

Author notes

  1. C. J. Condon

    Present address: Department of Psychology, University of California, Riverside, 92521, Riverside, CA, USA

Authors and Affiliations

  1. Department of Physiology and Biophysics, the Neuroscience Program, and the Beckman Institute, University of Illinois at Urbana-Champaign, 61801, Urbana, IL, USA

    C. J. Condon, K. R. White & A. S. Feng

Authors
  1. C. J. Condon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. R. White
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. S. Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Condon, C.J., White, K.R. & Feng, A.S. Neurons with different temporal firing patterns in the inferior colliculus of the little brown bat differentially process sinusoidal amplitude-modulated signals. J Comp Physiol A 178, 147–157 (1996). https://doi.org/10.1007/BF00188158

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00188158

Key words

Search

Navigation