Synaptic depression in the localization of sound

  • A Corrigendum to this article was published on 08 May 2003

Abstract

Short-term synaptic plasticity, which is common in the central nervous system, may contribute to the signal processing functions of both temporal integration and coincidence detection1,2,3. For temporal integrators, whose output firng rate depends on a running average of recent synaptic inputs, plasticity modulates input synaptic strength and thus may directly control signalling gain2 and the function of neural networks1,2,3,4. But the firing probability of an ideal coincidence detector would depend on the temporal coincidence of events rather than on the average frequency of synaptic events. Here we have examined a specific case of how synaptic plasticity can affect temporal coincidence detection, by experimentally characterizing synaptic depression at the synapse between neurons in the nucleus magnocellularis and coincidence detection neurons in the nucleus laminaris in the chick auditory brainstem5. We combine an empirical description of this depression with a biophysical model of signalling in the nucleus laminaris. The resulting model predicts that synaptic depression provides an adaptive mechanism for preserving interaural time-delay information (a proxy for the location of sound in space) despite the confounding effects of sound-intensity-related information. This mechanism may help nucleus laminaris neurons to pass specific sound localization information to higher processing centres.

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Figure 1: Synaptic depression at NM–NL synapses.
Figure 2: Simulating phase-locked NM synaptic input to NL neurons.
Figure 3: Distinctive firing properties of chick and model NL neurons.
Figure 4: Synaptic depression buffers coincidence detection against changing sound intensity.

References

  1. 1

    Tsodyks, M., Pawelzik, K. & Markram, H. Neural networks with dynamic synapses. Neural Comput. 10, 821–835 (1998)

    CAS  Article  Google Scholar 

  2. 2

    Abbott, L. F., Varela, J. A., Sen, K. & Nelson, S. B. Synaptic depression and cortical gain control. Science 275, 220–224 (1997)

    CAS  Article  Google Scholar 

  3. 3

    Dobrunz, L. E. & Stevens, C. F. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18, 995–1008 (1997)

    CAS  Article  Google Scholar 

  4. 4

    Nadim, F., Manor, Y., Kopell, N. & Marder, E. Synaptic depression creates a switch that controls the frequency of an oscillatory circuit. Proc. Natl Acad. Sci. USA 96, 8206–8211 (1999)

    ADS  CAS  Article  Google Scholar 

  5. 5

    Parks, T. N. & Rubel, E. W. Organization and development of brain stem auditory nuclei of the chicken: organization of projections from n. magnocellularis to n. laminaris. J. Comp. Neurol. 164, 435–448 (1975)

    CAS  Article  Google Scholar 

  6. 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)

    CAS  Article  Google Scholar 

  7. 7

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

    CAS  Article  Google Scholar 

  8. 8

    Carr, C. E. & Konishi, M. A circuit for detection of interaural time differences in the brain stem of the barn owl. J. Neurosci. 10, 3227–3246 (1990)

    CAS  Article  Google Scholar 

  9. 9

    Zhou, N. & Parks, T. N. Pharmacology of excitatory amino acid neurotransmission in nucleus laminaris of the chick. Hear. Res. 52, 195–200 (1991)

    CAS  Article  Google Scholar 

  10. 10

    Warchol, M. E. & Dallos, P. Neural coding in the chick cochlear nucleus. J. Comp. Physiol. A 166, 721–734 (1990)

    CAS  Article  Google Scholar 

  11. 11

    Pena, J. L., Viete, S., Albeck, Y. & Konishi, M. Tolerance to sound intensity of binaural coincidence detection in the nucleus laminaris of the owl. J. Neurosci. 16, 7046–7054 (1996)

    CAS  Article  Google Scholar 

  12. 12

    Reyes, A. D., Rubel, E. W. & Spain, W. J. In vitro analysis of optimal stimuli for phase-locking and time-delayed modulation of firing in avian nucleus laminaris neurons. J. Neurosci. 16, 993–1007 (1996)

    CAS  Article  Google Scholar 

  13. 13

    Funabiki, K., Koyano, K. & Ohmori, H. The role of GABAergic inputs for coincidence detection in the neurones of nucleus laminaris of the chick. J. Physiol. (Lond.) 508, 851–869 (1998)

    CAS  Article  Google Scholar 

  14. 14

    Bruckner, S. & Hyson, R. L. Effect of GABA on the processing of interaural time differences in nucleus laminaris neurons in the chick. Eur. J. Neurosci. 10, 3438–3450 (1998)

    CAS  Article  Google Scholar 

  15. 15

    Yang, L., Monsivais, P. & Rubel, E. W. The superior olivary nucleus and its influence on nucleus laminaris: a source of inhibitory feedback for coincidence detection in the avian auditory brainstem. J. Neurosci. 19, 2313–2325 (1999)

    CAS  Article  Google Scholar 

  16. 16

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

    ADS  CAS  Article  Google Scholar 

  17. 17

    Jackson, H. & Rubel, E. W. Ontogeny of behavioral responsiveness to sound in the chick embryo as indicated by electrical recordings of motility. J. Comp. Physiol. Psychol. 92, 682–696 (1978)

    CAS  Article  Google Scholar 

  18. 18

    Hines, M. L. & Carnevale, N. T. The NEURON simulation environment. Neural Comput. 9, 1179–1209 (1997)

    CAS  Article  Google Scholar 

  19. 19

    Koppl, C. Phase locking to high frequencies in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, Tyto alba. J. Neurosci. 17, 3312–3321 (1997)

    CAS  Article  Google Scholar 

  20. 20

    Lilly, A. W. & North, K. A. K. An electrical investigation of effects of repetitive stimulation on mammalian neuromuscular junction. J. Neurophysiol. 16, 509–527 (1953)

    Article  Google Scholar 

  21. 21

    Tsodyks, M. V. & Markram, H. The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc. Natl Acad. Sci. USA 94, 719–723 (1997)

    ADS  CAS  Article  Google Scholar 

  22. 22

    Brenowitz, S. & Trussell, L. O. Maturation of synaptic transmission at end-bulb synapses of the cochlear nucleus. J. Neurosci. 21, 9487–9498 (2001)

    CAS  Article  Google Scholar 

  23. 23

    Dobrunz, L. E., Huang, E. P. & Stevens, C. F. Very short-term plasticity in hippocampal synapses. Proc. Natl Acad. Sci. USA 94, 14843–14847 (1997)

    ADS  CAS  Article  Google Scholar 

  24. 24

    Harata, N. et al. Limited numbers of recycling vesicles in small CNS nerve terminals: implications for neural signaling and vesicular cycling. Trends Neurosci. 24, 637–643 (2001)

    CAS  Article  Google Scholar 

  25. 25

    von Gersdorff, H., Borst, J. & Gerard, G. Short-term plasticity at the calyx of Held. Nature Rev. Neurosci. 3, 55–64 (2002)

    Article  Google Scholar 

  26. 26

    Jeffress, L. A. Mathematical and electrical models of auditory detection. J. Acoust. Soc. Am. 44, 187–203 (1968)

    ADS  CAS  Article  Google Scholar 

  27. 27

    Tobias, J. V. & Zerlin, S. Lateralization thresholds as a function of stimulus duration. J. Acoust. Soc. Am. 31, 1591–1594 (1959)

    ADS  Article  Google Scholar 

  28. 28

    Wagner, H. A temporal window for lateralization of interaural time difference by barn owls. J. Comp. Physiol. A 169, 281–289 (1991)

    ADS  CAS  PubMed  Google Scholar 

  29. 29

    Smith, D. J. & Rubel, E. W. Organization and development of brain stem auditory nuclei of the chicken: dendritic gradients in nucleus laminaris. J. Comp. Neurol. 186, 213–239 (1979)

    CAS  Article  Google Scholar 

  30. 30

    Reyes, A. D., Rubel, E. W & Spain, W. J. Membrane properties underlying the firing of neurons in the avian cochlear nucleus. J. Neurosci. 14, 5352–5364 (1994)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank R. Lee for technical help and J. Simon for insight in using NEURON to model sound localization. This work was supported by a VA Merit Review and a grant from the National Institute for Deafness and Communication Disorders.

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Correspondence to William J. Spain.

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Cook, D., Schwindt, P., Grande, L. et al. Synaptic depression in the localization of sound. Nature 421, 66–70 (2003). https://doi.org/10.1038/nature01248

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