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.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Presynaptic endoplasmic reticulum regulates short-term plasticity in hippocampal synapses
Communications Biology Open Access 23 February 2021
-
Mesoscopic population equations for spiking neural networks with synaptic short-term plasticity
The Journal of Mathematical Neuroscience Open Access 06 April 2020
-
Different dynamical behaviors induced by slow excitatory feedback for type II and III excitabilities
Scientific Reports Open Access 27 February 2020
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout




References
Tsodyks, M., Pawelzik, K. & Markram, H. Neural networks with dynamic synapses. Neural Comput. 10, 821–835 (1998)
Abbott, L. F., Varela, J. A., Sen, K. & Nelson, S. B. Synaptic depression and cortical gain control. Science 275, 220–224 (1997)
Dobrunz, L. E. & Stevens, C. F. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18, 995–1008 (1997)
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)
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)
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)
Yin, T. C. & Chan, J. C. Interaural time sensitivity in medial superior olive of cat. J. Neurophysiol. 64, 465–488 (1990)
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)
Zhou, N. & Parks, T. N. Pharmacology of excitatory amino acid neurotransmission in nucleus laminaris of the chick. Hear. Res. 52, 195–200 (1991)
Warchol, M. E. & Dallos, P. Neural coding in the chick cochlear nucleus. J. Comp. Physiol. A 166, 721–734 (1990)
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)
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)
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)
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)
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)
Agmon-Snir, H., Carr, C. E. & Rinzel, J. The role of dendrites in auditory coincidence detection. Nature 393, 268–272 (1998)
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)
Hines, M. L. & Carnevale, N. T. The NEURON simulation environment. Neural Comput. 9, 1179–1209 (1997)
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)
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)
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)
Brenowitz, S. & Trussell, L. O. Maturation of synaptic transmission at end-bulb synapses of the cochlear nucleus. J. Neurosci. 21, 9487–9498 (2001)
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)
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)
von Gersdorff, H., Borst, J. & Gerard, G. Short-term plasticity at the calyx of Held. Nature Rev. Neurosci. 3, 55–64 (2002)
Jeffress, L. A. Mathematical and electrical models of auditory detection. J. Acoust. Soc. Am. 44, 187–203 (1968)
Tobias, J. V. & Zerlin, S. Lateralization thresholds as a function of stimulus duration. J. Acoust. Soc. Am. 31, 1591–1594 (1959)
Wagner, H. A temporal window for lateralization of interaural time difference by barn owls. J. Comp. Physiol. A 169, 281–289 (1991)
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)
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)
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing financial interests.
Supplementary information
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature01248
This article is cited by
-
Phase-change memtransistive synapses for mixed-plasticity neural computations
Nature Nanotechnology (2022)
-
Geometric characterization of dynamical structure for neural firing activities induced by inhibitory pulse
Cognitive Neurodynamics (2022)
-
Expression and Neurotransmitter Association of the Synaptic Calcium Sensor Synaptotagmin in the Avian Auditory Brain Stem
Journal of the Association for Research in Otolaryngology (2022)
-
Temporal filters in response to presynaptic spike trains: interplay of cellular, synaptic and short-term plasticity time scales
Journal of Computational Neuroscience (2022)
-
Presynaptic endoplasmic reticulum regulates short-term plasticity in hippocampal synapses
Communications Biology (2021)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.