Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex

Nature Neuroscience

Volumn 1, Issue 7, 1998, Pages 587-594

  Galarreta, Mario ^a   Hestrin, Shaul ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ANIMAL; ARTICLE; ELECTRIC CONDUCTIVITY; ELECTROSTIMULATION; HOMEOSTASIS; IN VITRO STUDY; METHODOLOGY; NEOCORTEX; NERVE CELL INHIBITION; PHYSIOLOGY; RAT; SYNAPSE; SYNAPTOSOME; TIME; WISTAR RAT;

ACTION POTENTIALS; ANIMALS; ELECTRIC CONDUCTIVITY; ELECTRIC STIMULATION; HOMEOSTASIS; NEOCORTEX; NEURAL INHIBITION; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; SYNAPSES; TIME FACTORS;

EID: 0032195844     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/2822     Document Type: Article

References (50)

1. Hubel, D. H. Single unit activity in striate cortex of unrestrained cats. J. Physiol (Lond.) 147, 226-238 (1959)
2. Mountcastle, V. B., Talbot, W. H., Sakata, H. & Hyvärinen, J. Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. J. Neurophysiol. 32, 452-458 (1969).
3. Hubel, D. H. & Wiesel, T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106-154 (1962).
4. Abeles, M. Corticonics. Neural Circuits of the Cerebral Cortex (Cambridge Univ. Press, Cambridge, 1991).
5. Azouz, R., Gray, C. M., Nowak, L. G. & McCormick, D. A. Physiological properties of inhibitory interneurons in cat striate cortex. Cereb. Cortex 7, 534-545 (1997).
6. White, E. L. Cortical Circuits (Birkhaüser, Boston, 1989).
7. Silva, L. R., Amitai, Y. & Connors, B. W. Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science 251, 432-435 (1991).
8. Shadlen, M. N. & Newsome, W. T. Noise, neural codes and cortical organization. Curr. Opin. Neurobiol 4, 569-579 (1994).
9. Buzsaki, G. & Chrobak, J. J. Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr. Opin. Neurobiol. 5, 504-510 (1995).
10. Somers, D. C. Nelson, S. B. & Sur, M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15, 5448-5465 (1995).
11. Douglas, R. J., Mahowald, M., Martin, K. A. & Stratford, K. J. The role of synapses in cortical computation. J. Neurocytol. 25, 893-911 (1996).
12. Konig, P., Engel, A. K. & Singer, W. Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 19, 130-137 (1996).
13. 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).
14. Abbott, L. F., Varela, J. A., Sen, K. & Nelson, S. B. Synaptic depression and cortical gain control. Science 275, 220-224 (1997).
15. Gutnick, M. J., Connors, B. W. & Prince, D. A. Mechanisms of neocortical epileptogenesis in vitro. J. Neurophysiol. 48, 1321-1335 (1982).
16. Somogyi., P., Kisvárday, Z. F., Martin, K. A. & Whitteridge, D. Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10, 261-294 (1983).
17. Kawaguchi, Y. Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J. Neurophysiol. 69, 416-431 (1993).
18. Thomson, A. M., West, D. C., Hahn, J. & Deuchars, J. Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex J. Physiol. (Lond.) 496, 81-102 (1996).
19. Tamás, G., Buhl, E. H. & Somogyi, P. Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. J. Physiol. (Lond.) 500, 715-738 (1997).
20. Thomson, A. M., Deuchars, J. & West, D. C. Single axon excitatory postsynaptic potentials in neocortical interneurons exhibit pronounced paired pulse facilitation. Neuroscience 54, 347-360 (1993).
21. Thomson, A. M. Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. J. Physiol. (Lond.) 502, 131-147 (1997).
22. Reyes, A. D. et al. Target-cell-specific facilitation and depression in neocortical circuits. Nature Neurosci. 1, 279-285 (1998).
23. Markram, H., Tsodyks, M. & Wang, Y. Differential signaling via the same axon of neocortical pyramidal neurons. Proc. Natl. Acad. Sci. USA 95, 5323-5328 (1998).
24. Porter, J. T. et al. Properties of bipolar VIPergic interneurones and their excitation by pyramidal neurons in the rat neocortex. Eur. J. Neurosci. (in press).
25. Tarczy-Hornoch, K., Martin, K. A., Jack, J. J. & Stratford, K. J. Synaptic interactions between smooth and spiny neurones in layer 4 of cat visual cortex in vitro. J. Physiol. (Lond.) 508, 351-363 (1998).
26. Zhang, S. & Trussell, L. O. Voltage clamp analysis of excitatory synaptic transmission in the avian nucleus magnocellularis. J. Physiol. (Lond.) 480, 123-136 (1994).
27. Takahashi, M., Kovalchuk, Y. & Attwell, D. Pre- and postsynaptic determinants of EPSC waveform at cerebellar climbing fiber and parallel fiber to Purkinje cell synapses. J. Neurosci. 15, 5693-5702 (1995)
28. Larkman, A. U., Jack, J. J. & Stratford, K. I. Quantal analysis of excitatory synapses in rat hippocampal CA1 in vitro during low-frequency depression. J. Physiol. (Lond.) 505, 457-471 (1997).
29. Partin, K. M., Patneau, D. K., Winters, C. A., Mayer, M. L. & Buonanno, A. Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 11, 1069-1082 (1993).
30. Pouzat, C. & Hestrin, S. Developmental regulation of basket/stellate cell→Purkinje cell synapses in the cerebellum. J. Neurosci. 17, 9104-9112 (1997).
31. Katz, B. Nerve, Muscle, and Synapse (McGraw Hill, New York, 1966).
32. Dobrunz, L. E. & Stevens, C. F. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18, 995-1008 (1997).
33. Liu, G. & Tsien, R. W. Properties of synaptic transmission at single hippocampal synaptic boutons. Nature 375, 404-408 (1995).
34. Ryan, T. A. & Smith, S. J. Vesicle pool mobilization during action potential firing at hippocampal synapses. Neuron 14, 983-989 (1995).
35. Stevens, C. F. & Tsujimoto, T. Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc. Natl Acad. Sci. USA 92, 846-849 (1995).
36. Shupliakov, O. et al. Synaptic vesicle endocytosis impaired by disruption of dynamin-H3 domain interactions. Science 276, 259-263 (1997).
37. von Gersdorff, H. & Matthews, G. Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal. J. Neurosci. 17, 1919-1927 (1997)
38. Neher, E. Vesicle pools and Ca2+ microdomains: New tools for understanding their roles in neurotransmitter release. Neuron 20, 389-399 (1998).
39. Wu, L. G. & Betz, W. J. Kinetics of synaptic depression and vesicle recycling after tetanic stimulation of frog motor nerve terminals. Biophys. J. 74, 3003-3009 (1998)
40. Klingauf, J, Kavalali, E. T. & Tsien, R. W. Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature 394, 581-585 (1998).
41. Silver, R. A., Momiyama, A. & Cull-Candy, S. G. Locus of frequency-dependent depression identified with multiple-probability fluctuation analysis at rat climbing fibre-Purkinje cell synapses. J. Physiol. (Lond.) 510, 881-902 (1998).
42. Wang, C. & Zucker, R. S. Regulation of synaptic vesicle recycling by calcium and serotonin. Neuron 21, 155-167 (1998).
43. Zucker, R. S. Short-term synaptic plasticity. Annu. Rev. Neurosci. 12, 13-31 (1989).
44. Forsythe, I. D., Tsujimoto, T., Barnes-Davies, M., Cuttle, M. F. & Takahashi, T. Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse. Neuron 20, 797-807 (1998).
45. Chance, F. S., Nelson, S. B. & Abbott, L. F. Synaptic depression and the temporal response characteristics of V1 cells. J. Neurosci. 18, 4785-4799 (1998).
46. Ohzawa, I., Sclar, G. & Freeman, R. D. Contrast gain control in the cat's visual system. J. Neurophysiol. 54, 651-667 (1985).
47. Moshon, J. A., Thompson, I. D. & Tolhurst, D. J. Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. J. Physiol. (Lond.) 283, 101-120 (1978).
48. Hawken, M. J., Shapley, R. M. & Grosof, D. H. Temporal-frequency selectivity in monkey visual cortex. Vis. Neurosci. 13, 477-492 (1996).
49. Carandini, M. & Ferster, D. A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. Science 276, 949-952 (1997).
50. Markram, H., Lübke, J., Frotscher, M., Roth, A. & Sakmann, B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J. Physiol. (Lond.) 500, 409-440 (1997).