Skip to main content
SpringerLink
Log in

Mechanisms for Analysis of Auditory Temporal Patterns in the Brainstem of Echolocating Bats

  • Chapter
Neural Representation of Temporal Patterns

Abstract

A vital function of the auditory system in all vertebrates is to identify sounds that are important for social interactions, predation and predator avoidance. Examples of these behaviorally important sounds are communication signals of conspecifics, noises made by movements of other animals and highly specialized species-specific sounds such as the biosonar signals used by echolocating bats. Identification of many behaviorally important sounds, especially those made by prey or predators, must occur rapidly to activate other neural systems that produce a motor response. Many biologically important sounds are characterized by simple temporal features, such as duration of the sound or its components, direction of a frequency sweep, or the rate of modulation in sounds that periodically change in frequency or amplitude. Many sounds are further characterized by complex sequences of elements that follow a specific order over time.

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

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 16.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Baron, G., 1974, Differential phylogenetic development of the acoustic nuclei among chiroptera, Brain Behav. Evol.,9:7.

    Article  PubMed  CAS  Google Scholar 

  • Buonomano and Merzenich, 1995, Temporal information transformed into a spatial code by a neural network with realistic properties, Science, 267:1028.

    Article  PubMed  CAS  Google Scholar 

  • Casseday, J.H. and Covey, E., 1992, Frequency tuning properties of neurons in the inferior colliculus of an FM bat, J. Comp. Neurol., 319: 34.

    Article  PubMed  CAS  Google Scholar 

  • Casseday, J.H. and Covey, E., 1995, A neuroethological theory of the operation of the inferior colliculus, Brain Behav. Evol., in press.

    Google Scholar 

  • Casseday, J.H., Ehrlich, D., and Covey, E., 1994, Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus, Science, 264:847.

    Article  PubMed  CAS  Google Scholar 

  • Condon, C.J., Chang, S.H., and Feng, A.S., 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., 168:709.

    Article  CAS  Google Scholar 

  • Covey, E. and Casseday, J.H., 1986, Connectional basis for frequency representation in the nuclei of the lateral lemniscus of the bat, Eptesicus fuscus, J. Neurosci., 6:2926.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Covey, E. and Casseday, J.H., 1995, The lower brainstem auditory pathways, in: “Springer Handbook of Auditory Research, vol 5, Hearing by Bats ”, A.N. Popper, and R.R. Fay, eds., Springer-Verlag, New York., NY.

    Google Scholar 

  • Covey, E., Johnson, B.R., Ehrlich, D., and Casseday, J.H., 1993, Neural representation of the temporal features of sound undergoes transformation at the auditory midbrain: Evidence from extracellular recording, application of pharmacological agents and in vivo whole cell patch clamp recording, Neurosci. Abstr. 19:535.

    Google Scholar 

  • Faingold, C.L., Boersma Anderson, C.A., and Caspary, D.M., 1991, Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons, Hear. Res., 52:201.

    Article  PubMed  CAS  Google Scholar 

  • Feng, A.S., Hall, J.C., and Gooler, D.M., 1990, Neural basis of sound pattern recognition in anurans, Prog. Neurobiol., 34:313.

    Article  PubMed  CAS  Google Scholar 

  • Fuzessery, Z.M., 1994, Response selectivity for multiple dimensions of frequency sweeps in the pallid bat inferior colliculus, J. Neurophysiol., 72:1061.

    PubMed  CAS  Google Scholar 

  • Glendenning, K.K. and Baker, B.N., 1988, Neuroanatomical distribution of receptors for three potential inhibitory neurotransmitters in the brainstem auditory nuclei of the cat, J. Comp. Neurol., 275:288.

    Article  PubMed  CAS  Google Scholar 

  • Godfrey, D.A., Carter, J.A., Lowry, O.H., and Matchinsky, F.M., 1978, Distribution of gama-aminobutyric acid, glycine, glutamate and aspartate in the cochlear nucleus of the rat, J. Histochem. Cytochem., 26:118.

    Article  PubMed  CAS  Google Scholar 

  • Goldberg, J.M. and Brown, P.B., 1969, Response of binaural neurons of dog superior olivary complex to dichotic tone stimuli: Some physiological mechanisms of sound localization, J. Neurophysiol., 32:613.

    PubMed  CAS  Google Scholar 

  • Gooler, D.M. and Feng, A.S., 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.

    PubMed  CAS  Google Scholar 

  • Grinnell, A.D., 1963a, The neurophysiology of audition in bats: intensity and frequency parameters, J. Physiol., 167:38.

    PubMed  CAS  Google Scholar 

  • Grinnell, A.D., 1963b, The neurophysiology of audition in bats: temporal parameters, J. Physiol, 167:67.

    PubMed  CAS  Google Scholar 

  • Grothe, B., Vater, M, Casseday, J. H., and Covey, E., 1992, Monaural interaction of excitation and inhibition in the medial superior olive of the mustached bat: an adaptation for biosonar, Proc. Nat. Acad. Sci., 89:5108.

    Article  PubMed  CAS  Google Scholar 

  • Hall, J.C. and Feng, A.S., 1991, Temporal processing in the dorsal medullary nucleus of the northern leopard frog (Rana pipiens pipiens), J. Neurophysiol., 66:955.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Havey, D.C., and Caspary, D.M., 1980, A simple technique for constructing “piggy-back” multibarrel microelectrodes. Electroencephalogr. Clin. Neurophysiol., 48:249–251.

    Article  CAS  Google Scholar 

  • Jeffress, L.A., 1948, A place theory of sound localization, J. Comp. Physiol Psychol, 41:35.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, B. R., 1993, GABAergic and Glycinergic Inhibition in the Central Nuclues of the Inferior Colliculus of the Big Brown Bat, Ph.D. dissertation, Duke University.

    Google Scholar 

  • Kalko, E.K.V. and Schnitzler, H.-U., 1989, The echolocation and hunting behavior of Daubenton’s bat, Myotis daubentoni, Behav. Ecol. Sociobiol., 24:225–238.

    Article  Google Scholar 

  • Kuwada, S., Batra, R., and Stanford, T.R., 1989, Monaural and binaural response properties of neurons in the inferior colliculus of the rabbit: Effects of sodium pentobarbital, J. Neurophysiol., 61:269.

    PubMed  CAS  Google Scholar 

  • Kuwada, S. and Yin, T.C.T., 1987, Physiological studies of directional hearing, in: “Directional Hearing ”, W.A. Yost and G. Gourevitch, eds., Springer, New York, NY.

    Google Scholar 

  • Licklider, J.C.R., 1951, A duplex theory of pitch perception, Experentia, 7:128.

    Article  CAS  Google Scholar 

  • Licklider, J.C.R., 1959, Three auditory theories, in: “ Psychology: A Study of a Science, Study I. Conceptual and Systematic, Vol. 1. Sensory, Perceptual, and Physiological Formulations ”, S. Koch, ed., McGraw-Hill, New York, NY.

    Google Scholar 

  • Middlebrooks, J.C., Clock, A.E., Xu, L, and Green, D.M., 1994, A panoramic code for sound location by cortical neurons, Science, 264:842.

    Article  PubMed  CAS  Google Scholar 

  • Narins, P.M. and Capranica, R.R., 1980, Neural adaptations for processing the two-note call of the Puerto Rican treefrog, Eleutherodactylus coqui, Brain Behav. Evol.,17:48.

    Article  CAS  Google Scholar 

  • Neuweiler, G., 1990, Auditory adaptations for prey capture in echolocating bats, Physiol. Rev., 70:615.

    PubMed  CAS  Google Scholar 

  • Park, T.J. and Pollak, G.D., 1993, GABA shapes a topographic organization of response latency in the mustache bat’s inferior colliculus, J. Neuroscl., 13:5172.

    CAS  Google Scholar 

  • Pinheiro, A.D., Wu, M., and Jen, P.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.

    Article  PubMed  CAS  Google Scholar 

  • Poljak, S., 1926, Untersuchungen am Oktavussystem der Säugetiere und an den mit diesem koordinierten motorischen Apparaten des Hirnstammes, J. Psychol. Neurol., 32:170.

    Google Scholar 

  • Pollak, G.D. and Casseday, J.H., 1989, “The Neural Basis of Echolocation in Bats ”, Springer-Verlag, Berlin.

    Book  Google Scholar 

  • Pollak, G.D. and Park, T.J., 1993, The effects of GABAergic inhibition on monaural response properties of neurons in the mustache bat’s inferior colliculus, Hear. Res., 65:99.

    Article  PubMed  CAS  Google Scholar 

  • Potter, H.D., 1965, Patterns of acoustically evoked discharges of neurons in the mesencephalon of the bullfrog, J. Neurophysiol., 28:1155.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Roberts, R.C. and Ribak, C.E., 1987, GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil, J. Comp. Neurol., 258:267.

    Article  PubMed  CAS  Google Scholar 

  • Rose, G.J. and Capranica, R.R., 1984, Processing amplitude-modulated sounds by the auditory midbrain of two species of toads: matched temporal filters, J. Comp. Physiol A, 154:211.

    Article  Google Scholar 

  • Rose, G.J. and Capranica, R.R., 1985, Sensitivity to amplitude modulated sounds in the anuran auditory nervous system, J. Neurophysiol., 53:446.

    PubMed  CAS  Google Scholar 

  • Rose, J.E., Greenwood, D.D., Goldberg, J.M., and Hind, J.E., 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.

    Google Scholar 

  • Ross, L.S. and Pollak, G.D., 1989, Differential ascending projections to aural regions in the 60 kHz contour of the mustache bat’s inferior colliculus, J. Neurosci., 9:2819.

    PubMed  CAS  Google Scholar 

  • Roverud, R.C. and Grinnell, A.D., 1985, Echolocation sound features processed to provide distance information in the CF/FM bat, Noctilio albiventris: evidence for a gated time window utilizing both CF and FM components, J. Comp. Physiol. A, (1985)156:457.

    Google Scholar 

  • Saint Marie, R., Ostapoff, E.M., Morest, D.K., and Wenthold, R.J., 1989, Glycine-immunoreactive projection of the cat lateral superior olive: possible role in midbrain ear dominance, J. Comp. Neurol, 279:382.

    Article  Google Scholar 

  • Schnitzler, H.-U., Kalko, E., Miller, L., and Surlykke, A., 1987, The echolocation and hunting behavior of the bat, Pipistrellus kuhli, J. Comp. Physiol A, 161:267.

    Article  PubMed  CAS  Google Scholar 

  • Schreiner, C.E. and Langner, G., 1988, Periodicity coding in the inferior colliculus of the cat. II. Topographical organization, J. Neurophysiol., 60:1823.

    PubMed  CAS  Google Scholar 

  • Schweizer, H., 1981, The connections of the inferior colliculus and the organization of the brainstem auditory system in the greater horseshoe bat (Rhinolophus ferrumequinum), J. Comp. Neurol, 201:25.

    Article  PubMed  CAS  Google Scholar 

  • Simmons, J.A., 1989, A view of the world through the bat’s ear: the formation of acoustic images in echolocation, Cognition, 33:155.

    Article  PubMed  CAS  Google Scholar 

  • Suga, N., 1964a, Single unit activity in cochlear nucleus and inferior colliculus of echo-locating bats, J. Physiol, 172:449.

    PubMed  CAS  Google Scholar 

  • Suga, N., 1964b, Recovery cycles and responses to frequency modulated tone pulses in auditory neurones of echo-locating bats, J. Physiol, 175:50.

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    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 (Lond.), 200:555.

    CAS  Google Scholar 

  • Suga, N., 1972, Analysis of information bearing elements in complex sounds by auditory neurons of bats, Audiology, 11:58.

    Article  Google Scholar 

  • Suga, N., 1973, Feature extraction in the auditory system of bats, in: “Basic Mechanisms in Hearing ”, A.R. Moller, ed., Academic Press, New York, NY.

    Google Scholar 

  • Suga, N., 1990, Cortical computational maps for auditory imaging. Neural Networks, 3:3.

    Article  Google Scholar 

  • Suga, N., and Schlegel, P., 1973, Coding and processing in the auditory systems of FM-signal-producing bats. J. Acoust. Soc. Am., 54:174.

    Article  PubMed  CAS  Google Scholar 

  • Vater, M., Casseday, J.H., and Covey, E., 1995, Convergence and divergence of ascending binaural and monaural pathways from the superior olives of the mustached bat, J. Comp. Neurol, 351:632.

    Article  PubMed  CAS  Google Scholar 

  • Vater, M., Habbicht, H., Kössl, M., and Grothe, B., 1992, The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats, J. Comp. Physiol A, 171:541.

    Article  PubMed  CAS  Google Scholar 

  • Von der Emde, G. and Schnitzler, H.-U., 1986, Fluttering target detection in Hipposiderid bats, J. Comp. Physiol, 159:765.

    Article  Google Scholar 

  • Wenthold, R.J., Zempel, J.M., Parakkal, M.H., Reeks, K.A., and Altschuler, R.A., 1986, Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig, Brain Res., 380:7.

    Article  PubMed  CAS  Google Scholar 

  • Yin, T.C.T. and Chan, J.C.K., 1990, Interaural time sensitivity in medial superior olive of cat, J. Neurophysioi., 64:465.

    CAS  Google Scholar 

  • Zook, J. M. and Casseday, J.H., 1982a, Cytoarchitecture of auditory system in lower brainstem of the mustache bat, Pteronotus parnellii, J. Comp. Neurol., 207:1.

    Article  PubMed  CAS  Google Scholar 

  • Zook, J. M. and Casseday, J.H., 1982b, Origin of ascending projections to inferior colliculus in the mustache bat, Pteronotus parnellii, J. Comp. Neurol, 207:14.

    Article  PubMed  CAS  Google Scholar 

  • Zook, J. M. and Casseday, J.H., 1985, Projections from the cochlear nuclei in the mustache bat, Pteronotus parnellii, J. Comp. Neurol, 237:307.

    Article  PubMed  CAS  Google Scholar 

  • Zook, J. M. and Casseday, J.H., 1987, Convergence of ascending pathways at the inferior colliculus in the mustache bat, Pteronotus parnellii, J. Comp. Neurol, 261:347.

    Article  PubMed  CAS  Google Scholar 

  • Zook, J.M., Jacobs, M.S., Glezer, I., and Morgane, P.J., 1988, Some comparative aspects of auditory brainstem cytoarchitecture in echolocating mammals: Speculations on the morphological basis of time-domain signal processing, in: “Animal Sonar: Processes and Performance ”, P.E. Nachtigall and P.W.B. Moore, eds., Plenum, New York, NY.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurobiology, Duke University Medical Center, Durham, NC, 27710, USA

    John H. Casseday & Ellen Covey

Authors
  1. John H. Casseday
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ellen Covey
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Duke University Medical Center, Durham, North Carolina, USA

    Ellen Covey

  2. Office of Naval Research, Arlington, Virginia, USA

    Harold L. Hawkins

  3. Indiana University, Bloomington, Indiana, USA

    Robert F. Port

Rights and permissions

Reprints and permissions

Copyright information

© 1995 Springer Science+Business Media New York

About this chapter

Cite this chapter

Casseday, J.H., Covey, E. (1995). Mechanisms for Analysis of Auditory Temporal Patterns in the Brainstem of Echolocating Bats. In: Covey, E., Hawkins, H.L., Port, R.F. (eds) Neural Representation of Temporal Patterns. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1919-5_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-1919-5_2

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-5785-8

  • Online ISBN: 978-1-4615-1919-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation