Abstract
In the dorsal cochlear nucleus, long-term synaptic plasticity can be induced at the parallel fiber inputs that synapse onto both fusiform principal neurons and cartwheel feedforward inhibitory interneurons. Here we report that in mouse fusiform cells, spikes evoked 5 ms after parallel-fiber excitatory postsynaptic potentials (EPSPs) led to long-term potentiation (LTP), whereas spikes evoked 5 ms before EPSPs led to long-term depression (LTD) of the synapse. The EPSP-spike protocol led to LTD in cartwheel cells, but no synaptic changes resulted from the reverse sequence (spike-EPSP). Plasticity in fusiform and cartwheel cells therefore followed Hebbian and anti-Hebbian learning rules, respectively. Similarly, spikes generated by summing EPSPs from different groups of parallel fibers produced LTP in fusiform cells, and LTD in cartwheel cells. LTD could also be induced in glutamatergic inputs of cartwheel cells by pairing parallel-fiber EPSPs with depolarizing glycinergic PSPs from neighboring cartwheel cells. Thus, synaptic learning rules vary with the postsynaptic cell, and may require the interaction of different transmitter systems.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 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
Young, E.D. & Davis, K.A. Circuitry and functions of the dorsal cochlear nucleus. in Integrative Functions of the Mammalian Auditory Pathway (eds. Oertel, D., Popper, A.N. & Fay, R.R.) 160–206 (Springer-Verlag, New York, 2002).
Oertel, D. & Young, E.D. What's a cerebellar circuit doing in the auditory system? Trends Neurosci. 27, 104–110 (2004).
Sutherland, D.P., Masterton, R.B. & Glendenning, K.K. Role of acoustic striae in hearing: reflexive responses to elevated sound-sources. Behav. Brain Res. 97, 1–12 (1998).
May, B.J. Role of the dorsal cochlear nucleus in the sound localization behavior of cats. Hear. Res. 148, 74–87 (2000).
Golding, N.L. & Oertel, D. Physiological identification of the targets of cartwheel cells in the dorsal cochlear nucleus. J. Neurophysiol. 78, 248–260 (1997).
Golding, N.L. & Oertel, D. Context-dependent synaptic action of glycinergic and GABAergic inputs in the dorsal cochlear nucleus. J. Neurosci. 16, 2208–2219 (1996).
Davis, K.A., Miller, R.L. & Young, E.D. Effects of somatosensory and parallel-fiber stimulation on neurons in dorsal cochlear nucleus. J. Neurophysiol. 76, 3012–3024 (1996).
Fujino, K. & Oertel, D. Bidirectional synaptic plasticity in the cerebellum-like mammalian dorsal cochlear nucleus. Proc. Natl. Acad. Sci. USA 100, 265–270 (2003).
Bell, C.C., Han, V.Z., Sugawara, Y. & Grant, K. Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387, 278–281 (1997).
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).
Markram, H., Lubke, J., Frotscher, M. & Sakmann, B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213–215 (1997).
Sjostrom, P.J., Turrigiano, G.G. & Nelson, S.B. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32, 1149–1164 (2001).
Han, V.Z., Grant, K. & Bell, C.C. Reversible associative depression and nonassociative potentiation at a parallel fiber synapse. Neuron 27, 611–622 (2000).
Roberts, P.D. & Bell, C.C. Computational consequences of temporally asymmetric learning rules: II. Sensory image cancellation. J. Comput. Neurosci. 9, 67–83 (2000).
Bell, C.C. Evolution of cerebellum-like structures. Brain Behav. Evol. 59, 312–326 (2002).
Manis, P.B., Spirou, G.A., Wright, D.D., Paydar, S. & Ryugo, D.K. Physiology and morphology of complex spiking neurons in the guinea pig dorsal cochlear nucleus. J. Comp. Neurol. 348, 261–276 (1994).
Zhang, S. & Oertel, D. Cartwheel and superficial stellate cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. J. Neurophysiol. 69, 1384–1397 (1993).
Debanne, D., Gahwiler, B.H. & Thompson, S.M. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J. Physiol. 507, 237–247 (1998).
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).
Molitor, S.C. & Manis, P.B. Dendritic Ca2+ transients evoked by action potentials in rat dorsal cochlear nucleus pyramidal and cartwheel neurons. J. Neurophysiol. 89, 2225–2237 (2003).
Berrebi, A.S. & Mugnaini, E. Distribution and targets of the cartwheel cell axon in the dorsal cochlear nucleus of the guinea pig. Anat. Embryol. 183, 427–454 (1991).
Ehrlich, I., Lohrke, S. & Friauf, E. Shift from depolarizing to hyperpolarizing glycine action in rat auditory neurones is due to age-dependent Cl− regulation. J. Physiol. 520, 121–137 (1999).
Maccaferri, G., Toth, K. & McBain, C.J. Target-specific expression of presynaptic mossy fiber plasticity. Science 279, 1368–1370 (1998).
Reyes, A. et al. Target-cell-specific facilitation and depression in neocortical circuits. Nat. Neurosci. 1, 279–285 (1998).
Sjostrom, P.J. & Nelson, S.B. Spike timing, calcium signals and synaptic plasticity. Curr. Opin. Neurobiol. 12, 305–314 (2002).
Magee, J.C. & Johnston, D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275, 209–213 (1997).
Zhang, L.I., Tao, H.W., Holt, C.E., Harris, W.A. & Poo, M. A critical window for cooperation and competition among developing retinotectal synapses. Nature 395, 37–44 (1998).
Egger, V., Feldmeyer, D. & Sakmann, B. Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex. Nat. Neurosci. 2, 1098–1105 (1999).
Tao, H.W., Zhang, L.I., Engert, F. & Poo, M. Emergence of input specificity of LTP during development of retinotectal connections in vivo. Neuron 31, 569–580 (2001).
Pouille, F. et al. Dendro-somatic distribution of calcium-mediated electrogenesis in Purkinje cells from rat cerebellar slice cultures. J. Physiol. 527, 265–282 (2000).
Neveu, D. & Zucker, R.S. Postsynaptic levels of [Ca2+]i needed to trigger LTD and LTP. Neuron 16, 619–629 (1996).
Lisman, J. A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc. Natl. Acad. Sci. USA 86, 9574–9578 (1989).
Ryugo, D.K., Pongstaporn, T., Wright, D.D. & Sharp, A.H. Inositol 1,4,5-trisphosphate receptors: immunocytochemical localization in the dorsal cochlear nucleus. J. Comp. Neurol. 358, 102–118 (1995).
Bilak, S.R. & Morest, D.K. Differential expression of the metabotropic glutamate receptor mGluR1alpha by neurons and axons in the cochlear nucleus: in situ hybridization and immunohistochemistry. Synapse 28, 251–270 (1998).
Molitor, S.C. & Manis, P.B. Voltage-gated Ca2+ conductances in acutely isolated guinea pig dorsal cochlear nucleus neurons. J. Neurophysiol. 81, 985–998 (1999).
Yao, H. & Dan, Y. Stimulus timing-dependent plasticity in cortical processing of orientation. Neuron 32, 315–323 (2001).
Chavas, J. & Marty, A. Coexistence of excitatory and inhibitory GABA synap1ses in the cerebellar interneuron network. J. Neurosci. 23, 2019–2031 (2003).
Veruki, M.L. & Hartveit, E. Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. J. Neurosci. 22, 10558–10566 (2002).
Beierlein, M., Gibson, J.R. & Connors, B.W. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat. Neurosci. 3, 904–910 (2000).
Rumsey, C.C. & Abbott, L.F. Equalization of synaptic efficacy by activity- and timing-dependent synaptic plasticity. J. Neurophysiol. 91, 2273–2280 (2004).
Acknowledgements
This work was supported by National Institutes of Health grant NS28901. We thank G. Awatramani, C. Bell, A. Klug, T. Lu and N. Golding for discussions about this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Rights and permissions
About this article
Cite this article
Tzounopoulos, T., Kim, Y., Oertel, D. et al. Cell-specific, spike timing–dependent plasticities in the dorsal cochlear nucleus. Nat Neurosci 7, 719–725 (2004). https://doi.org/10.1038/nn1272
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn1272
This article is cited by
-
Audiotactile interactions in the mouse cochlear nucleus
Scientific Reports (2021)
-
A calcium-influx-dependent plasticity model exhibiting multiple STDP curves
Journal of Computational Neuroscience (2020)
-
Burst synchronization in a scale-free neuronal network with inhibitory spike-timing-dependent plasticity
Cognitive Neurodynamics (2019)
-
Effects of Acoustic Paired Associative Stimulation on Late Auditory Evoked Potentials
Brain Topography (2019)