Skip to main content

Sound-evoked oscillation and paradoxical latency shift in the inferior colliculus neurons of the big fruit-eating bat, Artibeus jamaicensis

Journal of Comparative Physiology A volume 197, pages 1159–1172 (2011)Cite this article

Abstract

Frequency tuning, temporal response pattern and latency properties of inferior colliculus neurons were investigated in the big fruit-eating bat, Artibeus jamaicensis. Neurons having best frequencies between 48–72 kHz and between 24–32 kHz are overrepresented. The inferior colliculus neurons had either phasic (consisting in only one response cycle at all stimulus intensities) or long-lasting oscillatory responses (consisting of multiple response cycles). Seventeen percent of neurons displayed paradoxical latency shift, i.e. their response latency increased with increasing sound level. Three types of paradoxical latency shift were found: (1) stable, that does not depend on sound duration, (2) duration-dependent, that grows with increasing sound duration, and (3) progressive, whose magnitude increases with increasing sound level. The temporal properties of paradoxical latency shift neurons compare well with those of neurons having long-lasting oscillatory responses, i.e. median inter-spike intervals and paradoxical latency shift below 6 ms are overrepresented. In addition, oscillatory and paradoxical latency shift neurons behave similarly when tested with tones of different durations. Temporal properties of oscillation and PLS found in the IC of fruit-eating bats are similar to those found in the IC of insectivorous bats using downward frequency-modulated echolocation calls.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Abbreviations

BF:

Best frequency

FM:

Frequency modulated

IC:

Inferior colliculus

PLS:

Paradoxical latency shift

PSTH:

Post-stimulus time histogram

SPL:

Sound pressure level

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 

  • Brinkløv S, Kalko EKV, Surlykke A (2009) Intense echolocation calls from two ‘whispering’ bats, Artibeus jamaicensis and Macrophyllum macrophyllum (Phyllostomidae). J Exp Biol 212:11–20

    Article  PubMed  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(9):3009–3018

    PubMed  CAS  Google Scholar 

  • Esser KH, Eiermann A (1999) Tonotopic organization and parcellation of auditory cortex in the FM-bat Carollia perspicillata. Eur J Neurosci 11(10):3669–3682

    Article  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(4368):645–648

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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 

  • Gould E (1975) Neonatal vocalizations in bats of eight genera. J Mammal 56:15–29

    Article  PubMed  CAS  Google Scholar 

  • Griffin DR (1958) Listening in the Dark. Yale University Press, New Haven, CT (Reprinted by Dover Publications, New York, 1974, and Cornell Univ. Press, Ithaca, NY, 1986)

  • Hagemann C, Esser KH, Kössl M (2010) Chronotopically organized target-distance map in the auditory cortex of the short-tailed fruit bat. J Neurophysiol 103(1):322–333

    Article  PubMed  Google Scholar 

  • Hagemann C, Vater M, Kössl M (2011) Comparison of properties of cortical echo delay-tuning in the short-tailed fruit bat and the mustached bat. J Comp Physiol A 197(5):605–613

    Article  Google Scholar 

  • Harris R, Henze DA, Csicsvari J, Hirase H, Buzáki G (2000) Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J Neurophysiol 84:401–414

    PubMed  CAS  Google Scholar 

  • Heffner RS, Koay G, Heffner HE (2003) Hearing in American leaf-nosed bats. III: Artibeus jamaicensis. Hear Res 184(1–2):113–122

    Article  PubMed  Google Scholar 

  • Hoffmann S, Firzlaff U, Radtke-Schuller S, Schwellnus B, Schuller G (2008) The auditory cortex of the bat Phyllostomus discolor: Localization and organization of basic response properties. BMC Neurosci. doi:10.1186/1471-2202-9-65

  • Jones KE, Purvis A, MacLarnon A, Bininda-Emonds OR, Simmons NB (2002) A phylogenetic supertree of the bats (Mammalia: Chiroptera). Biol Rev Camb Philos Soc 77(2):223–259

    Article  PubMed  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 

  • Koay G, Bitter KS, Heffner HE, Heffner RS (2002) Hearing in American leaf-nosed bats. I: Phyllostomus hastatus. Hear Res 171(1–2):96–102

    Article  PubMed  Google Scholar 

  • Koay G, Heffner RS, Bitter KS, Heffner HE (2003) Hearing in American leaf-nosed bats. II: Carollia perspicillata. Hear Res 178(1–2):27–34

    Article  PubMed  Google Scholar 

  • Korine C, Kalko EKV (2005) Fruit detection and discrimination by small fruit-eating bats (Phyllostomidae): echolocation call design and olfaction. Behav Ecol Sociobiol 59:12–23

    Article  Google Scholar 

  • Lewicki MS (1998) A review of methods for spike sorting: the detection and classification of neural action potentials. Network 9(4):R53–R78

    Article  PubMed  CAS  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 

  • Macías S, Mora EC (2006) Adaptations in the echolocation call structure during foraging in the big fruit-eating bat Artibeus jamaicensis parvipes (Chiroptera, Phyllostomidae) in Cuba. Biología 20(1–2):24–29

    Google Scholar 

  • Mittmann DH, Wenstrup JJ (1995) Combination-sensitive neurons in the inferior colliculus. Hear Res 90(1–2):185–191

    Article  PubMed  CAS  Google Scholar 

  • Mora EC, Macías S, Vater M, Coro F, Kössl M (2004) Specializations for aerial hawking in the echolocation system of Molossus molossus (Molossidae, Chiroptera). J Comp Physiol A 190:561–574

    Article  CAS  Google Scholar 

  • Neuweiler G, Vater M (1977) Response patterns to pure tones of cochlear nucleus units in the CF-FM bat, Rhinolophus ferrumequinum. J Comp Physiol 115:119–133

    Article  Google Scholar 

  • O’Neill WE, Suga N (1979) Target range-sensitive neurons in the auditory cortex of the mustache bat. Science 203(4375):69–73

    Article  PubMed  Google Scholar 

  • Portfors CV, Wenstrup JJ (1999) Delay-tuned neurons in the inferior colliculus of the mustached bat: implications for analyses of target distance. J Neurophysiol 82(3):1326–1338

    PubMed  CAS  Google Scholar 

  • Schuller G, O’Neill WE, Radtke-Schuller S (1991) Facilitation and delay sensitivity of auditory cortex neurons in CF-FM bats, Rhinolophus rouxi and Pteronotus parnellii. Eur J Neurosci 3(11):1165–1181

    Article  PubMed  Google Scholar 

  • Sterbing SJ (2002) Postnatal development of vocalizations and hearing in the phyllostomid bat, Carollia perspicillata. J Mammal 83:516–525

    Article  Google Scholar 

  • Sterbing SJ, Schmidt U, Rübsamen R (1994) The postnatal development of frequency-place code and tuning characteristics in the auditory midbrain of the phyllostomid bat, Carollia perspicillata. Hear Res 76(1–2):133–146

    Article  PubMed  CAS  Google Scholar 

  • Sullivan WE (1982a) Neural representation of target distance in auditory cortex of the echolocating bat Myotis lucifugus. J Neurophysiol 48(4):1011–1032

    PubMed  Google Scholar 

  • Sullivan WE (1982b) Possible neural mechanisms of target distance coding in auditory system of the echolocating bat, Myotis lucifugus. J Neurophysiol 48(4):1033–1047

    PubMed  Google Scholar 

  • Thies W, Kalko EKV, Schnitzle HU (1998) The roles of echolocation and olfaction in two Neotropical fruit-eating bats, Carollia perspicillata and C. castanea, feeding on Piper. Behav Ecol Sociobiol 42:397–409

    Article  Google Scholar 

  • Vater M, Schlegel P (1979) Comparative auditory neurophysiology of the inferior colliculus of two molossid bats Molossus ater and Molossus molossus II. Single unit responses to frequency-modulated signals and signal and noise combinations. J Comp Physiol A 131:147–160

    Article  Google Scholar 

  • Voytenko SV, Galazyuk AV (2008) Timing of sound-evoked potentials and spike responses in the inferior colliculus of awake bats. Neuroscience 155(3):923–936

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Galazyuk AV, Feng AS (2007) FM signals produce robust paradoxical latency shifts in the bat’s inferior colliculus. J Comp Physiol A 193(1):13–20

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank the Alexander von Humboldt Foundation (Germany) and to the German Academic Exchange Service (DAAD) for support. The animal use in this study was authorized by the Center for the Inspection and Control of the Environment, of the Cuban Ministry of Science, Technology, and Environment and is in accordance with the Declaration of Helsinki.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Animal and Human Biology, University of Havana, Havana, Cuba

    Julio C. Hechavarría, Ariadna T. Cobo, Yohami Fernández, Silvio Macías & Emanuel C. Mora

  2. Institut für Zellbiologie und Neurowissenschaft, Goethe-Universität, Siesmayerstrasse 70A, 60323, Frankfurt/Main, Germany

    Julio C. Hechavarría & Manfred Kössl

Authors
  1. Julio C. Hechavarría
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ariadna T. Cobo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yohami Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Silvio Macías
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Manfred Kössl
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Emanuel C. Mora
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Julio C. Hechavarría.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hechavarría, J.C., Cobo, A.T., Fernández, Y. et al. Sound-evoked oscillation and paradoxical latency shift in the inferior colliculus neurons of the big fruit-eating bat, Artibeus jamaicensis . J Comp Physiol A 197, 1159–1172 (2011). https://doi.org/10.1007/s00359-011-0678-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-011-0678-x

Keywords

  • Big fruit-eating bat (Artibeus jamaicensis)
  • Inferior colliculus (IC)
  • Frequency tuning
  • Oscillation
  • Paradoxical latency shift (PLS)