Skip to main content
Log in

FM signals produce robust paradoxical latency shifts in the bat’s inferior colliculus

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

Abstract

Previous studies in echolocating bats, Myotis lucifugus, showed that paradoxical latency shift (PLS) is essential for neural computation of target range and that a number of neurons in the inferior colliculus (IC) exhibit unit-specific PLS (characterized by longer first-spike latency at higher sound levels) in response to tone pulses at the unit’s best frequency. The present study investigated whether or not frequency-modulated (FM) pulses that mimic the bat’s echolocation sonar signals were equally effective in eliciting PLS. For two-thirds of PLS neurons in the IC, both FM and tone pulses could elicit PLS, but only FM pulses consistently produced unit-specific PLS. For the remainder of PLS neurons, only FM pulses effectively elicited PLS; these cells showed either no PLS or no response, to tone pulses. PLS neurons generally showed more pronounced PLS in response to narrow-band FM (each sweeping 20 kHz in 2 ms) pulse that contained the unit’s best frequency. In addition, almost all PLS neurons showed duration-independent PLS to FM pulses, but the same units exhibited duration-dependent PLS to tone pulses. Taken together, when compared to tone pulses, FM stimuli can provide more reliable estimates of target range.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Berkowitz A, Suga N (1989) Neural mechanisms of ranging are different in two species of bats. Hear Res 41:255–264

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Casseday JH, Covey E (1992) Frequency tuning properties of neurons in the inferior colliculus of an FM bat. J Comp Neurol 319:34–50

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Casseday JH, Covey E, Grothe B (1997) Neural selectivity and tuning for sinusoidal frequency modulations in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Neurophysiol 77:1595–1605

    PubMed  CAS  Google Scholar 

  • Covey E (1993) Response properties of single units in the dorsal nucleus of the lateral lemniscus and paralemniscal zone of an echolocating bat. J Neurophysiol 69:842–859

    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 77:2360–2370

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick DC, Suga N, Misawa H (1991) Are the initial frequency-modulated components of the mustached bat’s biosonar pulses important for ranging? J Neurophysiol 66:951–964

    Google Scholar 

  • Fuzessery ZM (1994) Response selectivity for multiple dimensions of frequency sweeps in the pallid bat inferior colliculus. J Neurophysiol 72(3):1061–1079

    PubMed  CAS  Google Scholar 

  • Fuzessery ZM, Hall JC (1996) Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. J Neurophysiol 76:1059–1073

    PubMed  CAS  Google Scholar 

  • Galazyuk AV, Feng AS (2001) Oscillation may play a role in time domain central auditory processing. J Neurosci 21(RC147):1–5

    Google Scholar 

  • Galazyuk AV, Lin W, Llano D, Feng AS (2005) Leading inhibition to neural oscillation is important for time-domain processing in the auditory midbrain. J Neurophysiol 94:314–326

    Article  PubMed  Google Scholar 

  • Ghose K, Moss CF (2003) The sonar beam pattern of a flying bat as it tracks tethered insects. J Acoust Soc Am 114:1120–1131

    Article  PubMed  Google Scholar 

  • Gordon M, O’Neill WE (2000) An extralemniscal component of the mustached bat inferior colliculus selective for direction and rate of linear frequency modulations. J Comp Neurol 426:165–181

    Article  PubMed  CAS  Google Scholar 

  • Klug A, Khan A, Burger RM, Bauer EE, Hurley LM, Yang L, Grothe B, Halvorsen MB, Park TJ (2000) Latency as a function of intensity in auditory neurons: influences of central processing. Hear Res 148:107–123

    Article  PubMed  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 CE (1988) Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. J Neurophysiol 60:1799–1822

    PubMed  CAS  Google Scholar 

  • Maekawa M, Wong D, Paschal WG (1992) Spectral selectivity of FM–FM neurons in the auditory cortex of the echolocating bat, Myotis lucifugus. J Comp Physiol A171:513–522

    Google Scholar 

  • Mittmann DH, Wenstrup JJ (1995) Combination-sensitive neurons in the inferior colliculus. Hear Res 90:185–191

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • O’Neill WE (1995) The bat auditory cortex. In: Popper AN, Fay RR (eds) Hearing by bats. Springer, Berlin Heidelberg New York, pp 416–498

    Google Scholar 

  • O’Neill WE, Brimijoin WO (2002) Directional selectivity for FM sweeps in the suprageniculate nucleus of the mustached bat medial geniculate body. J Neurophysiol 88:172–187

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Olsen JF, Suga N (1991b) Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of relative velocity information. J Neurophysiol 65:1254–1274

    CAS  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 A169:69–85

    Google Scholar 

  • Poon PW, Chen X, Cheung YM (1992) Differences in FM response correlate with morphology of neurons in the rat inferior colliculus. Exp Brain Res 91:94–104

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Roverud RC (1993) Neural computations for sound pattern recognition: evidence for summation of an array of frequency filters in an echolocating bat. J Neurosci 13:2306–2312

    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 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Shannon-Hartman S, Wong D, Maekawa M (1992) Processing of pure-tone and FM stimuli in the auditory cortex of the FM bat, Myotis lucifugus. Hear Res 61:179–188

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Simmons JA (1979) Perception of echo phase information in bat sonar. Science 204:1336–1338

    Article  PubMed  CAS  Google Scholar 

  • Suga N (1965) Analysis of frequency modulated sounds by neurons of echolocating bats. J Physiol 179:26–53

    PubMed  CAS  Google Scholar 

  • Suga N (1968) Analysis of frequency modulated and complex sounds by single auditory neurons of bats. J Physiol 198:51–80

    PubMed  CAS  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 200:555–574

    PubMed  CAS  Google Scholar 

  • Suga N, O’Neill WE, Kujirai K, Manabe T (1983) Specificity of combination-sensitive neurons for processing of complex biosonar signals in auditory cortex of the mustached bat. J Neurophysiol 49:1573–1626

    PubMed  CAS  Google Scholar 

  • Sullivan WE (1982a) Neural representation of target distance in auditory cortex of the echolocating bat Myotis lucifugus. J Neurophysiol 48:1011–1032

    Google Scholar 

  • Sullivan WE (1982b) Possible neural mechanisms of target distance coding in auditory system of the echolocating bat Myotis lucifugus. J Neurophysiol 48:1033–1047

    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 108:2419–2429

    Article  PubMed  CAS  Google Scholar 

  • Wadsworth J, Moss CF (2000) Vocal control of acoustic information for sonar discriminations by the echolocating bat, Eptesicus fuscus. J Acoust Soc Am 107:2265–2271

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This research is supported by a grant from the National Institute on Deafness and Communication Disorders of the NIH (R01DC04998). We thank Wenyu Lin and Karla Melendez for their comments on earlier versions of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xinming Wang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, X., Galazyuk, A.V. & Feng, A.S. FM signals produce robust paradoxical latency shifts in the bat’s inferior colliculus. J Comp Physiol A 193, 13–20 (2007). https://doi.org/10.1007/s00359-006-0167-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-006-0167-9

Keywords

Navigation