Quantal events shape cerebellar interneuron firing

Nature Neuroscience

Volumn 5, Issue 12, 2002, Pages 1309-1318

  Carter, Adam G ^a   Regehr, Wade G ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CONTROLLED STUDY; INTERNEURON; NONHUMAN; PRIORITY JOURNAL; RAT; STELLATE CELL; SYNAPSE; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CEREBELLAR CORTEX; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; INTERNEURONS; NEURAL INHIBITION; NEURAL PATHWAYS; POTASSIUM CHANNELS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 0036897560     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn970     Document Type: Article

References (50)

1. Buzsaki, G. & Chrobak, J. J. Temporal structure in spatially organized neuronal ensembles: A role for interneuronal networks. Curr. Opin. Neurobiol. 5, 504-510 (1995).
2. McBain, C. J. & Fisahn, A. Interneurons unbound. Nat. Rev. Neurosci. 2, 11-23 (2001).
3. Abeles, M. Corticonics: Neural Circuits of the Cerebral Cortex (Cambridge Univ. Press, Cambridge, UK, 1991).
4. Softky, W. R. & Koch, C. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J. Neurosci. 13, 334-350 (1993).
5. Shadlen, M. N. & Newsome, W. T. Noise, neural codes and cortical organization. Curr. Opin. Neurobiol. 4, 569-579 (1994).
6. Eccles, J. C. The Physiology of Nerve Cells (Johns Hopkins Press, Baltimore, Maryland, 1957).
7. Sayer, R. J., Redman, S. J. & Andersen, P. Amplitude fluctuations in small EPSPs recorded from CA1 pyramidal cells in the guinea pig hippocampal slice. J. Neurosci. 9, 840-850 (1989).
8. Mason, A., Nicoll, A. & Stratford, K. Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro. J. Neurosci. 11, 72-84 (1991).
9. Eccles, J. C., Llinas, R. & Sasaki, K. The excitatory synaptic action of climbing fibers on the Pukinje cells of the cerebellum. J. Physiol. 182, 268-296 (1966).
10. Cleland, B. G., Dubin, M. W. & Levick, W. R. Simultaneous recording of input and output of lateral geniculate neurones. Nat. New Biol. 231, 191-192 (1971).
11. Zhang, S. & Trussell, L. O. A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J. Neurophysiol. 72, 705-718 (1994).
12. Fetz, E. E. & Gustafsson, B. Relation between shapes of post-synaptic potentials and changes in firing probability of cat motoneurones. J. Physiol. 341, 387-410 (1983).
13. Barbour, B. Synaptic currents evoked in Purkinje cells by stimulating individual granule cells. Neuron 11, 759-769 (1993).
14. Miles, R. Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig in vitro. J. Physiol. 428, 61-77 (1990).
15. Bennett, B. D. & Wilson, C. J. Synaptic regulation of action potential timing in neostriatal cholinergic interneurons. J. Neurosci. 18, 8539-8549 (1998).
16. Fricker, D. & Miles, R. EPSP amplification and the precision of spike timing in hippocampal neurons. Neuron 28, 559-569 (2000).
17. Galarreta, M. & Hestrin, S. Spike transmission and synchrony detection in networks of GABAergic interneurons. Science 292, 2295-2299 (2001).
18. Oertel, D. The role of intrinsic neuronal properties in the encoding of auditory information in the cochlear nuclei. Curr. Opin. Neurobiol. 1, 221-228 (1991).
19. Miles, R. & Wong, R. K. S. Excitatory synaptic interactions between CA3 neurones in the guinea-pig hippocampus. J. Physiol. 373, 397-418 (1986).
20. Pouille, F. & Scanziani, M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293, 1159-1163 (2001).
21. Geiger, J. R., Lubke, J., Roth, A., Frotscher, M. & Jonas, P. Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18, 1009-1023 (1997).
22. Mann-Metzer, P. & Yarom, Y. Jittery trains induced by synaptic-like currents in cerebellar inhibitory interneurons. J. Neurophysiol. 87, 149-156 (2002).
23. Midtgaard, J. Membrane properties and synaptic responses of Golgi cells and stellate cells in the turtle cerebellum in vitro. J. Physiol. 457, 329-354 (1992).
24. Bennett, B. D., Callaway, J. C. & Wilson, C. J. Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J. Neurosci. 20, 8493-8503 (2000).
25. Reyes, A. D. & Fetz, E. E. Two modes of interspike interval shortening by brief transient depolarizations in cat neocortical neurons. J. Neurophysiol. 69, 1661-1672 (1993).
26. Abeles, M. Role of the cortical neuron: Integrator or coincidence detector? Isr. J. Med. Sci. 18, 83-92 (1982).
27. Mainen, Z. F. & Sejnowski, T. J. Reliability of spike timing in neocortical neurons. Science 268, 1503-1506 (1995).
28. Stevens, C. F. & Zador, A. M. Input synchrony and the irregular firing of cortical neurons. Nat. Neurosci. 1, 210-217 (1998).
29. Palay, S. L. & Chan-Palay, V. Cerebellar Cortex p. 348 (Springer-Verlag, New York, 1974).
30. Llano, I. & Gerschenfeld, H. M. Inhibitory synaptic currents in the stellate cells of rat cerebellar slices. J. Physiol. 468, 177-200 (1993).
31. 2+]i increases in the dendrites of cerebellar Purkinje neurons. J. Neurosci. 15, 2777-2787 (1995).
32. Midtgaard, J. Stellate cell inhibition of Purkinje cells in the turtle cerebellum in vitro. J. Physiol. 457, 355-367 (1992).
33. Hausser, M. & Clark, B. A. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19, 665-678 (1997).
34. Jaeger, D. & Bower, J. M. Synaptic control of spiking in cerebellar Purkinje cells: Dynamic current clamp based on model conductances. J. Neurosci. 19, 6090-6101 (1999).
35. Robinson, H. P. & Kawai, N. Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons. J. Neurosci. Methods 49, 157-165 (1993).
36. Sharp, A. A., O'Neil, M. B., Abbott, L. F. & Marder, E. Dynamic damp: Computer-generated conductances in real neurons. J. Neurophysiol. 69, 992-995 (1993).
37. Kreitzer, A. C., Carter, A. G. & Regehr, W. G. Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum. Neuron 34, 787-796 (2002).
38. Eccles, J. C., Llinas, R. & Sasaki, K. The inhibitory interneurones within the cerebellar cortex. Exp. Brain Res. 1, 1-16 (1966).
39. Carter, A. G. & Regehr, W. G. Prolonged synaptic currents and glutamate spillover at the parallel fiber to stellate cell synapse. J. Neurosci. 20, 4423-4434 (2000).
40. Nusser, Z., Naylor, D. & Mody, I. Synapse-specific contribution of the variation of transmitter concentration to the decay of inhibitory postsynaptic currents. Biophys. J. 80, 1251-1261 (2001).
41. Armstrong, D. M. & Rawson, J. A. Activity patterns of cerebellar cortical neurones and climbing fibre afferents in the awake cat. J. Physiol. 289, 425-448 (1979).
42. Sui, J. L., Chan, K., Langan, M. N., Vivaudou, M. & Logothetis, D. E. G protein gated potassium channels. Adv. Second Messenger Phosphoprotein Res. 33, 179-201 (1999).
43. Mark, M. D. & Herlitze, S. G-protein mediated gating of inward-rectifier K+ channels. Eur. J. Biochem. 267, 5830-5836 (2000).
44. Otmakhov, N., Shirke, A. M. & Malinow, R. Measuring the impact of probabilistic transmission on neuronal output. Neuron 10, 1101-1111 (1993).
45. Kondo, S. & Marty, A. Synaptic currents at individual connections among stellate cells in rat cerebellar slices. J. Physiol. 509, 221-232 (1998).
46. Gulyas, A. I., Miles, R., Hajos, N. & Freund, T. F. Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur. J. Neurosci. 5, 1729-1751 (1993).
47. Miles, R., Toth, K., Gulyas, A. I., Hajos, N. & Freund, T. F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16, 815-823 (1996).
48. Koch, C. Biophysics of Computation (Oxford Univ. Press, New York, 1999).
49. Ito, M. The Cerebellum and Neural Control p. 580 (Raven Press, New York, 1984).
50. Auger, C. & Marty, A. Heterogeneity of functional synaptic parameters among single release sites. Neuron 19, 139-150 (1997).