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Experience-dependent refinement of inhibitory inputs to auditory coincidence-detector neurons

Nature Neuroscience volume 5, pages 247–253 (2002)Cite this article

Abstract

The spatial arrangement of inputs on to single neurons is assumed to be crucial in accurate signal processing. In mammals, the most precise temporal processing occurs in the context of sound localization. Medial superior olivary neurons can encode microsecond differences in the arrival time of low-frequency sounds at the two ears. Here we show that in mammals with well developed low-frequency hearing, a spatial refinement of ionotropic inhibitory inputs occurs on medial superior olivary neurons during development. This refinement is experience dependent and does not develop in mammals that do not use interaural time differences for sound localization.

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Figure 1: Arrangement of functional inputs to the MSO.
Figure 2: Glycinergic inputs are confined to somata in adult gerbil MSO but not in juvenile and cochlear-ablated gerbils.
Figure 3: Glycine receptor distribution on gerbil MSO neurons.
Figure 4: Electron micrographs showing ultrastructural localization of inhibitory, glycinergic synapses on gerbil MSO cell bodies (CB) and cross-sectioned dendrites (D).
Figure 5: Quantification of the spatial arrangement of glycinergic inputs on gerbil MSO neurons.
Figure 6: Glycinergic inputs on MSO neurons of only high frequency–hearing animals.

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References

  1. Häusser, M., Spruston, N. & Stuart, G. J. Diversity and dynamics of dendritic signaling. Science 290, 739–744 (2000).

    Article  PubMed  Google Scholar 

  2. Craig, A. M., Blackstone, C. D., Huganir, R. L. & Banker, G. The distribution of glutamate receptors in cultured rat hippocampal neurons: postsynaptic clustering of AMPA-selective subunits. Neuron 10, 1055–1068 (1993).

    Article  CAS  PubMed  Google Scholar 

  3. Lin, B., Martin, P. R., Solomon, S. G. & Grunert, U. Distribution of glycine receptor subunits on primate retinal ganglion cells: a quantitative analysis. Eur. J. Neurosci. 12, 4155–4170 (2000).

    CAS  PubMed  Google Scholar 

  4. Nyiri, G., Freund, T. F. & Somogyi, P. Input-dependent synaptic targeting of α2-subunit-containing GABAA receptors in synapses of hippocampal pyramidal cells of the rat. Eur. J. Neurosci. 13, 428–442 (2001).

    Article  CAS  PubMed  Google Scholar 

  5. Erulkar, S. D. Comparative aspects of sound localization. Physiol. Rev. 52, 237–360 (1972).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  7. Yin, T. C. & Chan, J. C. Interaural time sensitivity in medial superior olive of cat. J. Neurophysiol. 64, 465–488 (1990).

    Article  CAS  PubMed  Google Scholar 

  8. Grothe, B. The evolution of temporal processing in the medial superior olive, an auditory brainstem structure. Prog. Neurobiol. 61, 581–610 (2000).

    Article  CAS  PubMed  Google Scholar 

  9. Inbody, S. B. & Feng, A. S. Binaural response characteristics of single neurons in the medial superior olivary nucleus of the albino rat. Brain Res. 210, 361–366 (1981).

    Article  CAS  PubMed  Google Scholar 

  10. Grothe, B. & Park, T. J. Sensitivity to interaural time differences in the medial superior olive of a small mammal, the Mexican free-tailed bat. J. Neurosci. 18, 6608–6622 (1998).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Joris, P. X., Smith, P. H. & Yin, T. C. Coincidence detection in the auditory system: 50 years after Jeffress. Neuron 21, 1235–1238 (1998).

    Article  CAS  PubMed  Google Scholar 

  12. Cant, N. B. & Hyson, R. L. Projections from the lateral nucleus of the trapezoid body to the medial superior olivary nucleus in the gerbil. Hear. Res. 58, 26–34 (1992).

    Article  CAS  PubMed  Google Scholar 

  13. Grothe, B. & Sanes, D. H. Synaptic inhibition influences the temporal coding properties of medial superior olivary neurons: an in vitro study. J. Neurosci. 14, 1701–1709 (1994).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Agmon-Snir, H., Carr, C. E. & Rinzel, J. The role of dendrites in auditory coincidence detection. Nature 393, 268–272 (1998).

    Article  CAS  PubMed  Google Scholar 

  15. Simon, J. Z., Carr, C. E. & Shamma, S. A. A dendritic model of coincidence detection in the avian brainstem. Neurocomputing 26–27, 263–269 (1999).

    Article  Google Scholar 

  16. Spitzer, M. W. & Semple, M. N. Neurons sensitive to interaural phase disparity in gerbil superior olive: diverse monaural and temporal response properties. J. Neurophysiol. 73, 1668–1690 (1995).

    Article  CAS  PubMed  Google Scholar 

  17. Smith, P. H., Joris, P. X. & Yin, T. C. Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: evidence for delay lines to the medial superior olive. J. Comp. Neurol. 331, 245–260 (1993).

    Article  CAS  PubMed  Google Scholar 

  18. Russell, F. A. & Moore, D. R. Afferent reorganisation within the superior olivary complex of the gerbil: development and induction by neonatal, unilateral cochlear removal. J. Comp. Neurol. 35, 607–625 (1995).

    Article  Google Scholar 

  19. Smith, P. H., Joris, P. X. & Yin, T. C. Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. J. Neurophysiol. 79, 3127–3142 (1998).

    Article  CAS  PubMed  Google Scholar 

  20. Taschenberger, H. & von Gersdorff, H. Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J. Neurosci. 20, 9162–9173 (2000).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Heffner, R. S. & Heffner, H. E. Sound localization and use of binaural cues by the gerbil (Meriones unguiculatus). Behav. Neurosci. 102, 422–428 (1988).

    Article  CAS  PubMed  Google Scholar 

  22. Kneussel, O. M. & Betz, H. Receptors, gephyrin and gephyrin-associated proteins: novel insights into the assembly of inhibitory postsynaptic membrane specializations. J. Physiol. 525, 1–9 (2000).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Sanes, D. H. The development of synaptic function and integration in the central auditory system. J. Neurosci. 13, 2627–2637 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Sanes, D. H., Markowitz, S., Bernstein, J. & Wardlow, J. The influence of inhibitory afferents on the development of postsynaptic dendritic arbors. J. Comp. Neurol. 321, 637–344 (1992).

    Article  CAS  PubMed  Google Scholar 

  26. Withington-Wray, D. J., Binns, K. E., Dhanjal, S. S., Brickley, S. G. & Keating, M. J. The maturation of the superior collicular map of auditory space in the guinea pig is disrupted by developmental auditory deprivation. Eur. J. Neurosci. 2, 693–703 (1990).

    Article  PubMed  Google Scholar 

  27. Vater, M. Ultrastructural and immunocytochemical observations on the superior olivary complex of the mustached bat. J. Comp. Neurol. 358, 155–180 (1995).

    Article  CAS  PubMed  Google Scholar 

  28. Clark, G. M. The ultrastructure of nerve endings in the medial superior olive of the cat. Brain Res. 14, 293–305 (1969).

    Article  CAS  PubMed  Google Scholar 

  29. Perkins, R. E. An electron microscopic study of synaptic organization in the medial superior olive of normal and experimental chinchillas. J. Comp. Neurol. 148, 387–415 (1973).

    Article  CAS  PubMed  Google Scholar 

  30. Langford, T. L. Responses elicited from medial superior olivary neurons by stimuli associated with binaural masking and unmasking. Hear. Res. 15, 39–50 (1984).

    Article  CAS  PubMed  Google Scholar 

  31. Pouille, F. & Scanziani, M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293, 1159–1163 (2001).

    Article  CAS  PubMed  Google Scholar 

  32. Suneja, S. K., Benson, C. G. & Potashner, S. J. Glycine receptors in adult guinea pig brain stem auditory nuclei: regulation after unilateral cochlear ablation. Exp. Neurol. 154, 473–488 (1998).

    Article  CAS  PubMed  Google Scholar 

  33. Lichtman, J. W. & Colman, H. Synapse elimination and indelible memory. Neuron 25, 269–278 (2000).

    Article  CAS  PubMed  Google Scholar 

  34. Keller-Peck, C. R. et al. Asynchronous synapse elimination in neonatal motor units: studies using GFP transgenic mice. Neuron 31, 381–394 (2001).

    Article  CAS  PubMed  Google Scholar 

  35. Katz, L. C. & Shatz, C. J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996).

    Article  CAS  PubMed  Google Scholar 

  36. Chapman, B., Jacobson, M. D., Reiter, H. O. & Stryker, M. P. Ocular dominance shift in kitten visual cortex caused by imbalance in retinal electrical activity. Nature 324, 154–156 (1986).

    Article  CAS  PubMed  Google Scholar 

  37. Kakizawa, S., Yamasaki, M., Watanabe, M. & Kano, M. Critical period for activity-dependent synapse elimination in developing cerebellum. J. Neurosci. 20, 4954–4961 (2000).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Ichise, T. et al. mGluR1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Science 288, 832–1835 (2000).

    Article  Google Scholar 

  39. O'Leary, D. D., Ruff, N. L. & Dyck, R. H. Development, critical period plasticity, and adult reorganizations of mammalian somatosensory systems. Curr. Opin. Neurobiol. 4, 535–544 (1994).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  41. Rietzel, H. J. & Friauf, E. Neuron types in the rat lateral superior olive and developmental changes in the complexity of their dendritic arbors. J. Comp. Neurol. 390, 20–40 (1998).

    Article  CAS  PubMed  Google Scholar 

  42. Sanes, D. H. & Rubel, E. W. The ontogeny of inhibition and excitation in the gerbil lateral superior olive. J. Neurosci. 8, 682–700 (1988).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Craig, A. M., Blackstone, C. D., Huganir, R. L. & Banker, G. Selective clustering of glutamate and γ-aminobutyric acid receptors opposite terminals releasing the corresponding neurotransmitters. Proc. Natl. Acad. Sci. USA 91, 12373–12377 (1994).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Komatsu, Y. GABAB receptors, monoamine receptors, and postsynaptic inositol trisphosphate–induced Ca2+ release are involved in the induction of long-term potentiation at visual cortical inhibitory synapses. J. Neurosci. 16, 6342–6352 (1996).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Alvarez, F. J., Dewey, D. E., Harrington, D. A. & Fyffe, R. E. Cell-type specific organization of glycine receptor clusters in the mammalian spinal cord. J. Comp. Neurol. 379, 150–170 (1997).

    Article  CAS  PubMed  Google Scholar 

  46. Bi, G. Q. & Poo, M. M. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18, 10464–10472 (1998).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Feldman, D. E. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27, 45–56 (2000).

    Article  CAS  PubMed  Google Scholar 

  48. Kotak, V. C. & Sanes, D. H. Long-lasting inhibitory synaptic depression is age- and calcium-dependent. J. Neurosci. 20, 5820–5826 (2000).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgements

We thank U. Koch and O. Gleich for technical advice; C. Schulte, G. Breutel and D. Büringer for technical help; and M. Götz, T. Bonhoeffer, M. Hübener, A. Kossel, G. Neuweiler, T. Park and H. Thoenen for critical comments on the manuscript. Supported by Max-Planck-Gesellschaft and Deutsche Forschungsgemeinschaft (GR1205/10-1).

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Authors and Affiliations

  1. Max-Planck-Institute of Neurobiology, Am Klopferspitz 18a, Martinsried, 82152, Germany

    Christoph Kapfer, Armin H. Seidl & Benedikt Grothe

  2. Zoologisches Institut der Universität München, Luisenstrasse 14, München, 80333, Germany

    Hermann Schweizer

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Correspondence to Benedikt Grothe.

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Kapfer, C., Seidl, A., Schweizer, H. et al. Experience-dependent refinement of inhibitory inputs to auditory coincidence-detector neurons. Nat Neurosci 5, 247–253 (2002). https://doi.org/10.1038/nn810

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