Skip to main content
SpringerLink
Log in

Inhibitory and Excitatory Brainstem Connections Involved in Sound Localization: How do they Develop?

  • Chapter
Acoustical Signal Processing in the Central Auditory System

Abstract

Interaural time differences and interaural intensity differences are the two major cues that enable vertebrates to localize the direction of a sound source. Small mammalian species with a correspondingly small head width (distance between the two pinna ca. 2-4 cm), such as most rodents, do not experience interaural time differences longer than 60-120 us and, therefore, they generally rely on interaural intensity differences (IID). High frequency hearing in the ultrasound range, which is common to these small animals, is advantageous to localize sound sources, because the wave lengths of ultrasounds are too short to bend around the head and because sound shadowing by the head becomes better with increasing sound frequency.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover 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

  • Altman, J. and Bayer, S.A. (1980) Development of the brain stem in the rat. III. Thymidine-radiographic study of the time of origin of neurons of the vestibular and auditory nuclei of the upper medulla. J. Comp. Neurol. 194, 877–904.

    Article  PubMed  CAS  Google Scholar 

  • Aoki, E., Semba, R., Keino, H., Kato, K. and Kashiwamata, S. (1988) Glycine-like immunoreactivity in the rat auditory pathway. Brain. Res. 442, 63–71.

    Article  PubMed  CAS  Google Scholar 

  • Aprison, M.H., Galvezruano, E., Robertson, D.H. and Lipkowitz, K.B. (1996) Glycine and GABA receptors: Molecular mechanisms controlling chloride ion flux. J. Neurosci. Res. 43, 372–381.

    Article  PubMed  CAS  Google Scholar 

  • Backus, K.H. and Friauf, E. (1996) Effects of synchronous depolarization on glycine-induced currents in developing rat auditory brainstem neurons. Soc. Neurosci. Abstr. 256, 6.

    Google Scholar 

  • Barker, J.L., McBurncy, R.N. and MacDonald, R.L. (1982) Fluctuation analysis of neutral amino acid responses in cultured mouse spinal neurones. J. Physiol. (Lond). 322, 365–387.

    CAS  Google Scholar 

  • Batini, C., Palestini, M., Thomassct, M. and Vigot, R. (1993) Cytoplasmic calcium buffer, calbindin-D28k, is regulated by excitatory amino acids. Neuroreport 4, 927–930.

    Article  PubMed  CAS  Google Scholar 

  • Ben-Ari, Y., Tseeb, V., Raggozzino, D., Khazipov, R. and Gaiarsa, J.L. (1994) y-Aminobutyric acid (GABA): a fast excitatory transmitter which may regulate the development of hippocampal neurones in early postnatal life. Prog. Brain. Res. 102, 261–273.

    Article  PubMed  CAS  Google Scholar 

  • Blatchley, B.J., Cooper, W.A. and Coleman, J.R. (1987) Development of auditory brainstem response to tone pip stimuli in the rat. Dev. Brain. Res. 32, 75–84.

    Article  Google Scholar 

  • Bledsoe, S.C.J., Snead, C.R., Helfert, R.H., Prasad, V., Wenthold, R.J. and Altschuler, R.A. (1990) Immunocyto-chemical and lesion studies support the hypothesis that the projection from the medial nucleus of the trape-zoid body to the lateral superior olive is glycinergic. Brain. Res. 517, 189–194.

    Article  PubMed  Google Scholar 

  • Boudreau, J.C. and Tsuchitani, C. (1968) Binaural interaction in the cat superior olive S segment. J. Neurophysiol. 31, 442–454.

    PubMed  CAS  Google Scholar 

  • Brown, R.D. and Feldman, A.M. (1978) Pharmacology of hearing and ototoxicity. Annu. Rev. Pharmacol. Toxicol. 18, 233–252.

    Article  PubMed  CAS  Google Scholar 

  • Caird, D. and Klinke, R. (1983) Processing of binaural stimuli by cat superior olivary complex neurons. Exp. Brain. Res. 52, 385–399.

    Article  PubMed  CAS  Google Scholar 

  • Chard, P.S., Bleakman, D., Christakos, S., Fullmer, C.S. and Miller, R.J. (1993) Calcium buffering properties of calbindin-D28k and parvalbumin in rat sensory neurones. J. Physiol. (Lond). 472, 341–357.

    CAS  Google Scholar 

  • Cherubini, E., Rovira, C., Gaiarsa, J.L., Corradetti, R. and Ben-Ari, Y. (1990) GABA mediated excitation in imma-ture rat CA3 hippocampal neurons. Int. J. Dev. Neurosci. 8, 481–490.

    Article  PubMed  CAS  Google Scholar 

  • Cherubini, E., Gaiarsa, J.L. and Ben-Ari, Y. (1991 ) GABA: an excitatory transmitter in early postnatal life. Trends. Neurosci. 14, 515–519.

    Article  PubMed  CAS  Google Scholar 

  • Constantine-Paton, M., CIine, H.T. and Debski, E. (1990) Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annu. Rev. Neurosci. 13, 129–154.

    Article  PubMed  CAS  Google Scholar 

  • Fox, K. and Zahs, K. (1994) Critical period control in sensory cortex. Curr. Opin. Neurobiol. 4, 112–119.

    Article  PubMed  CAS  Google Scholar 

  • Friauf, E. (1993) Transient appearance of calbindin-D28k-positive neurons in the superior olivary complex of de-veloping rats. J. Comp. Neurol. 334, 59–74.

    Article  PubMed  CAS  Google Scholar 

  • Friauf, E., Hammerschmidt, B., Kirsch, J. and Betz. H. (1994) Development of glycine receptor distribution in the rat auditory brainstem: transition from the ‘neonatal’ to the ‘adult’ isoform. Assoc. Res. Otolaryngol. Abstr. 17, 10.

    Google Scholar 

  • Friauf, E., Hammerschmidt, B. and Kirsch, J. (1997) Development of adult-type glycine receptors in the central auditory system of rats. J. Comp. Neurol. (in press).

    Google Scholar 

  • Friauf, E., Kandler, K. (1993) Cell birth, formation of efferent connections, and establishment of tonotopic order in the rat cochlear nucleus. In: MA. Merchán, J.M. Juiz, D.A. Godfrey and E. Mugnaini (Eds.), The Mammalian Cochlear Nuclei: Organization and Function, Plenum, New York, pp. 19–28.

    Chapter  Google Scholar 

  • Gao, B.X. and Ziskind-Conhaim, L. (1995) Development of glycine-and GABA-gated currents in rat spinal mo-toneurons. J. Neurophysiol. 74, 113–121.

    PubMed  CAS  Google Scholar 

  • Goldberg, J.M. and Brown, P.B. (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: Some physiological mechanism of sound localization. J. Neurophysiol. 32, 613–636.

    PubMed  CAS  Google Scholar 

  • Goodman, C.S. and Shatz, C.J. (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Neuron 10, 77–98.

    Google Scholar 

  • Guian, J.J.J., Norris, B.E. and Guinan, S.S. (1972) Single auditory units in the superior olivary complex. 11: Locations of unit categories and tonotopic organization. Int. J. Neurosci. 4, 147–166.

    Article  Google Scholar 

  • Hebb, D.O. (1949) The Organization of Behavior. John Wiley and Sons; New York.

    Google Scholar 

  • Helfert, R.H., Juiz, J.M., Bledsoe, S.C., Bonneau, J.M., Wenthold, R.J. and Altschuler, R.A. (1992) Patterns of glutamate, glycine, and GABA immunolabeling in four synaptic terminal classes in the lateral superior olive of the guinea pig. J. Comp. Neurol. 323, 305–325.

    Article  PubMed  CAS  Google Scholar 

  • Janigro, D. and Schwartzkroin, P.A. (1988) Effects of GABA and baclofen on pyramidal cells in the developing rabbit hippocampus: an ‘in vitro’ study. Dev. Brain. Res. 41, 171–184.

    Article  CAS  Google Scholar 

  • Kandler, K. and Friauf, E. (1993) Pre-and postnatal development of efferent connections of the cochlear nucleus in the rat. J. Comp. Neurol. 328, 161–184.

    Article  PubMed  CAS  Google Scholar 

  • Kandler, K. and Friauf, E. (1995) Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J. Neurosci. 15, 6890–6904.

    PubMed  CAS  Google Scholar 

  • Kelly. J.B. (1992) Behavioral development of the auditory orientation response. In: R. Romand (Ed.), Development of Auditory and Vestibular Systems 2, Elsevier, Amsterdam, London, New York, Tokyo, pp. 391–418.

    Google Scholar 

  • Kungel, M. and Friauf, E. (1996) Patch-clamp studies of auditory brainstem neurons: Developmental changes in physiology and glycinergic pharmacology. 1. Kongress der Neurowiss. Gesellschaft, Berlin.

    Google Scholar 

  • Langosch, D., Becker, C.-M. and Betz, H. (1990) The inhibitory glycine receptor: A ligand-gated chloride channel of the central nervous system. Eur. J. Biochem. 194, 1–8.

    Article  PubMed  CAS  Google Scholar 

  • Leinekugel, X., Tseeb, V., Ben-Ari, Y. and Bregestovski, P. (1995) Synaptic GABAA activation induces Ca2+ rise in pyramidal cells and interneurons from rat neonatal hippocampal slices. J. Physiol. (Lond). 487, 319–329.

    CAS  Google Scholar 

  • Lin. M.H., Takahashi, M.P., Takahashi, Y. and Tsumoto, T. (1994) Intracellular calcium increase induced by GABA in visual cortex of fetal and neonatal rats and its disappearance with development. Neurosci. Res. 20, 85–94.

    Article  PubMed  CAS  Google Scholar 

  • Lohmann, C. and Friauf, E. (1996) Distribution of the calcium-binding proteins parvalbumin and calretinin in the auditory brainstem of adult and developing rats. J. Comp. Neurol. 367, 90–109.

    Article  PubMed  CAS  Google Scholar 

  • Lohmann, C. and Friauf, E. (1997) An organotypic slice culture from a network of developing inhibitory and exci-tatory connections. Submitted.

    Google Scholar 

  • Loturco, J.J., Owens, D.F., Heath, M.J.S., Davis, M.B.E. and Kriegstein, A.R. (1995) GABA and glutamate depo-larize cortical progenitor cells and inhibit DNA synthesis. Neuron 15, 1287–1298.

    Article  PubMed  CAS  Google Scholar 

  • Luhmann, H.J. and Prince, D.A. (1991) Postnatal maturation of the GABAergic system in rat neocortex. J. Neurophysiol. 65, 247–263.

    PubMed  CAS  Google Scholar 

  • Lux, H.D. (1971) Ammonium and chloride extrusion: hyperpolarizing synaptic inhibition in spinal motoneurons. Science 173, 555–557.

    Article  PubMed  CAS  Google Scholar 

  • Miller, M.W. and Nowakowski, R.S. (1988) Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the entrai nervous system. Brain. Res. 457, 44–52.

    Article  PubMed  CAS  Google Scholar 

  • Misgeld, U., Deisz, R.A., Dodt, H.U. and Lux, H.D. (1986) The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 232, 1413–1415.

    Article  PubMed  CAS  Google Scholar 

  • Moore, D.R. (1992) Trophic influences of excitatory and inhibitory synapses on neurones in the auditory brain stem. Neuroreport 3, 269–272.

    Article  PubMed  CAS  Google Scholar 

  • Mueller, A.L., Taube, J.S. and Schwartzkroin, P.A. (1984) Development of hyperpolarizing inhibitory postsynaptic potentials and hyperpolarizing response to t-aminobutyric acid in rabbit hippocampus studied in vitro. J. Neurosci. 4, 860–867.

    PubMed  CAS  Google Scholar 

  • Nicoll, R.A. and Alger, B.E. (1980) Presynaptic inhibition: Transmitterand ionic mechanisms. Annu. Rev. Neurosci. 3, 227–268.

    Article  PubMed  CAS  Google Scholar 

  • Nishi, S., Minota, S. and Karczmar, A.G. (1974) Primary afferent neurones: The ionic mechanism of GABA-medi-ated depolarization. Neuropharmacology 13, 215–219.

    Article  PubMed  CAS  Google Scholar 

  • O’Leary. D.D.M., Ruff, N.L. and Dyck, R.H. (1994) Development, critical period plasticity, and adult reorganiza-tions of mammalian somatosensory systems. Curr. Opin. Neurobiol. 4, 535–544.

    Article  PubMed  Google Scholar 

  • Obata, K., Oide, M. and Tanaka, H. (1978) Excitatory and inhibitory actions of GABAand glycine on embryonic chick spinal neurons in culture. Brain. Res. 144, 179–184.

    Article  PubMed  CAS  Google Scholar 

  • Obrietan, K. and van den Pol, A.N. (1995) GABA neurotransmission in the hypothalamus: developmental reversal from Ca2+ elevating to depressing. J. Neurosci. 15, 5065–5077.

    PubMed  CAS  Google Scholar 

  • Obrietan, K. and van den Pol, A.N. (1996) Growth cone calcium elevation by GABA. J. Comp. Neurol. 372, 167–175.

    Article  PubMed  CAS  Google Scholar 

  • Owens, D.F., Boyce, L.H., Davis, M.B.E. and Kriegstein, A.R. (1996) Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J. Neurosci. 16, 6414–6423.

    PubMed  CAS  Google Scholar 

  • Puel, J.L. and Uziel, A. (1987) Correlative development of cochlear action potential sensitivity, latency, and frequency selectivity. Brain. Res. 465, 179–188.

    PubMed  CAS  Google Scholar 

  • Reichling, D.B., Kyrozis, A., Wang, J. and Mac Dermott, A.B. (1994) Mechanisms of GABAand glycine depolari-zation-induced calcium transients in rat dorsal horn neurons. J. Physiol. (Lond). 476, 411–421.

    CAS  Google Scholar 

  • Rietzel, H.-J., Friauf, E. (1995) Development of dendritic morphology in the rat auditory brainstem: bipolar and multipolar cells in the lateral superior olive. In: N. Eisner, R. Menzel (Eds.), Proc.G#x00F6;ttingen Neuro-biol.Conf. Vol. 23, Thieme Verlag, Stuttgart

    Google Scholar 

  • Sanes, D.H., Goldstein, N.A., Ostad, M. and Hillman, D.E. (1990) Dendritic morphology of central auditory neu-rons correlates with their tonotopic position. J. Comp. Neurol. 294, 443–454.

    Article  PubMed  CAS  Google Scholar 

  • Sanes, D.H., Markowitz, S., Bernstein, J. and Wardlow, J. (1992) The influence of inhibitory affrents on the development of postsynaptic dendritic arbors. J. Comp. Neurol. 321, 637–644.

    Article  PubMed  CAS  Google Scholar 

  • Sanes, D.H. and Chokshi, P. (1992) Glycinergic transmission influences the development of dendrite shape. Neuroreport 3, 323–326.

    Article  PubMed  CAS  Google Scholar 

  • Sanes, D.H. and Takacs, C. (1993) Activity-dependent refinement of inhibitory connections. Eur. J. Neurosci. 5, 570–574.

    Article  PubMed  CAS  Google Scholar 

  • Schmanns, H. and Friauf, E. (1994) K+-and transmitter-induced rises in [Ca2+], in auditory neurones of developing rats. Neuroreport 5, 2321–2324.

    Article  PubMed  CAS  Google Scholar 

  • Schwartz, R.D. and Yu, X. (1995) Optical imaging of intracellular chloride in living brain slices. J. Neurosci. Methods 62, 185–192.

    Article  PubMed  CAS  Google Scholar 

  • Sega, M. (1993) GABA induces a unique rise of [Ca]i in cultured rat hippocampal neurons. Hippocampus 3, 229–238.

    Article  Google Scholar 

  • Shatz, C.J. (1994) Role for spontaneous neural activity in the patterning of connections between retina and LGN during visual system development. Int. J. Dev. Neurosci. 12, 531–546.

    Article  PubMed  CAS  Google Scholar 

  • Suneja, S.K., Benson, C.G., Gross, J. and Potashner, S.J. (1995) Evidence for glutamatergic projections from the cochlear nucleus to the superior olive and the ventral nucleus of the lateral lemniscus. J. Neurochem. 64, 161–171.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, S.M., Deisz, R.A. and Prince, D.A. (1988) Outward chloride/cation co-transport in mammalian cortical neurons. Neurosci. Lett. 89, 49–54.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, S.M., Deisz, R.A. and Prince, D.A. (1989) Relative contributions of passive equilibrium and active transport to the distribution of chloride in mammalian cortical neurons. J. Neurophysiol. 60, 105–124.

    Google Scholar 

  • Tsuchitani, C. (1977) Functional organization of lateral cell groups of cat superior olivary complex. J. Neurophysiol. 40, 296–318.

    PubMed  CAS  Google Scholar 

  • Uziel, A., Romand, R. and Marot, M. (1981) Development of cochlear potentials in rats. Audiology 20, 89–100.

    Article  PubMed  CAS  Google Scholar 

  • Wang, J., Reichling, D.B., Kyrozis, A. and Mac Dermott, A.B. (1994) Developmental loss of GABA-and glycine-induced depolarization and Ca2+ transients in embryonic rat dorsal horn neurons in culture. Eur. J. Neuro-sci. 6, 1275–1280.

    Article  CAS  Google Scholar 

  • Weber, F., Zulus, H., Friauf, E. (1991) Neuronal birth in the rat auditory brainstem. In: N. Eisner, W. Singer (Eds.), Synapse, Transmission, Modulation. Proceedings of the 19th G#x00F6;ttingen Neurobiology Conference, Georg Thieme Verlag, Stuttgart, New York, pp. 123

    Google Scholar 

  • Wu, S.H. and Kelly, J.B. (1992) Synaptic pharmacology of the superior olivary complex studied in mouse brain slice. J. Neurosci. 12, 3084–3097.

    PubMed  CAS  Google Scholar 

  • Wu, W.I., Ziskind-Conhaim, L. and Sweet, M.A. (1992) Early development of glycine-and GABA-mediated synapses in rat spinal cord. J. Neurosci. 12, 3935–3945.

    PubMed  CAS  Google Scholar 

  • Yuste, R. and Katz. L.C. (1991) Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6, 333–344.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, L., Spigelman, I. and Carlen, P.L. (1991) Development of GABA-mediated, chloride-dependent inhibition of CAI pyramidal neurones of immature rat hippocampal slices. J. Physiol. (Lond). 444, 25–49.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zentrum der Physiologie, Klinikum der Universität Frankfurt, Theodor-Stern-Kai 7, D-60590, Frankfurt, Germany

    Eckhard Friauf, Karl Kandler, Christian Lohmann & Martin Kungel

Authors
  1. Eckhard Friauf
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karl Kandler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Lohmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Martin Kungel
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Academy of Sciences of the Czech Republic, Prague, Czech Republic

    Josef Syka

Rights and permissions

Reprints and permissions

Copyright information

© 1997 Springer Science+Business Media New York

About this chapter

Cite this chapter

Friauf, E., Kandler, K., Lohmann, C., Kungel, M. (1997). Inhibitory and Excitatory Brainstem Connections Involved in Sound Localization: How do they Develop?. In: Syka, J. (eds) Acoustical Signal Processing in the Central Auditory System. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-8712-9_17

Download citation

  • DOI: https://doi.org/10.1007/978-1-4419-8712-9_17

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-4673-9

  • Online ISBN: 978-1-4419-8712-9

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation