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. 1999 Feb;76(2):670–678. doi: 10.1016/S0006-3495(99)77234-6

Simultaneous induction of pathway-specific potentiation and depression in networks of cortical neurons.

Y Jimbo 1, T Tateno 1, H P Robinson 1
PMCID: PMC1300072  PMID: 9929472

Abstract

Activity-dependent modification of synaptic efficacy is widely recognized as a cellular basis of learning, memory, and developmental plasticity. Little is known, however, of the consequences of such modification on network activity. Using electrode arrays, we examined how a single, localized tetanic stimulus affects the firing of up to 72 neurons recorded simultaneously in cultured networks of cortical neurons, in response to activation through 64 different test stimulus pathways. The same tetanus produced potentiated transmission in some stimulus pathways and depressed transmission in others. Unexpectedly, responses were homogeneous: for any one stimulus pathway, neuronal responses were either all enhanced or all depressed. Cross-correlation of responses with the responses elicited through the tetanized site revealed that both enhanced and depressed responses followed a common principle: activity that was closely correlated before tetanus with spikes elicited through the tetanized pathway was enhanced, whereas activity outside a 40-ms time window of correlation to tetanic pathway spikes was depressed. Response homogeneity could result from pathway-specific recurrently excitatory circuits, whose gain is increased or decreased by the tetanus, according to its cross-correlation with the tetanized pathway response. The results show how spatial responses following localized tetanic stimuli, although complex, can be accounted for by a simple rule for activity-dependent modification.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ahissar E., Vaadia E., Ahissar M., Bergman H., Arieli A., Abeles M. Dependence of cortical plasticity on correlated activity of single neurons and on behavioral context. Science. 1992 Sep 4;257(5075):1412–1415. doi: 10.1126/science.1529342. [DOI] [PubMed] [Google Scholar]
  2. Bliss T. V., Collingridge G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 1993 Jan 7;361(6407):31–39. doi: 10.1038/361031a0. [DOI] [PubMed] [Google Scholar]
  3. Bliss T. V., Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol. 1973 Jul;232(2):331–356. doi: 10.1113/jphysiol.1973.sp010273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burgard E. C., Hablitz J. J. Developmental changes in NMDA and non-NMDA receptor-mediated synaptic potentials in rat neocortex. J Neurophysiol. 1993 Jan;69(1):230–240. doi: 10.1152/jn.1993.69.1.230. [DOI] [PubMed] [Google Scholar]
  5. Castro-Alamancos M. A., Donoghue J. P., Connors B. W. Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex. J Neurosci. 1995 Jul;15(7 Pt 2):5324–5333. doi: 10.1523/JNEUROSCI.15-07-05324.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Douglas R. J., Koch C., Mahowald M., Martin K. A., Suarez H. H. Recurrent excitation in neocortical circuits. Science. 1995 Aug 18;269(5226):981–985. doi: 10.1126/science.7638624. [DOI] [PubMed] [Google Scholar]
  7. Engert F., Bonhoeffer T. Synapse specificity of long-term potentiation breaks down at short distances. Nature. 1997 Jul 17;388(6639):279–284. doi: 10.1038/40870. [DOI] [PubMed] [Google Scholar]
  8. Fitzsimonds R. M., Song H. J., Poo M. M. Propagation of activity-dependent synaptic depression in simple neural networks. Nature. 1997 Jul 31;388(6641):439–448. doi: 10.1038/41267. [DOI] [PubMed] [Google Scholar]
  9. Hansel C., Artola A., Singer W. Different threshold levels of postsynaptic [Ca2+]i have to be reached to induce LTP and LTD in neocortical pyramidal cells. J Physiol Paris. 1996;90(5-6):317–319. doi: 10.1016/s0928-4257(97)87906-5. [DOI] [PubMed] [Google Scholar]
  10. Kamioka H., Maeda E., Jimbo Y., Robinson H. P., Kawana A. Spontaneous periodic synchronized bursting during formation of mature patterns of connections in cortical cultures. Neurosci Lett. 1996 Mar 15;206(2-3):109–112. doi: 10.1016/s0304-3940(96)12448-4. [DOI] [PubMed] [Google Scholar]
  11. Katz L. C., Shatz C. J. Synaptic activity and the construction of cortical circuits. Science. 1996 Nov 15;274(5290):1133–1138. doi: 10.1126/science.274.5290.1133. [DOI] [PubMed] [Google Scholar]
  12. Linden D. J. Long-term synaptic depression in the mammalian brain. Neuron. 1994 Mar;12(3):457–472. doi: 10.1016/0896-6273(94)90205-4. [DOI] [PubMed] [Google Scholar]
  13. Luhmann H. J., Prince D. A. Postnatal maturation of the GABAergic system in rat neocortex. J Neurophysiol. 1991 Feb;65(2):247–263. doi: 10.1152/jn.1991.65.2.247. [DOI] [PubMed] [Google Scholar]
  14. Maeda E., Robinson H. P., Kawana A. The mechanisms of generation and propagation of synchronized bursting in developing networks of cortical neurons. J Neurosci. 1995 Oct;15(10):6834–6845. doi: 10.1523/JNEUROSCI.15-10-06834.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Markram H., Lübke J., Frotscher M., Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science. 1997 Jan 10;275(5297):213–215. doi: 10.1126/science.275.5297.213. [DOI] [PubMed] [Google Scholar]
  16. McCormick D. A., Prince D. A. Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. J Physiol. 1987 Dec;393:743–762. doi: 10.1113/jphysiol.1987.sp016851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. McNaughton B. L. The mechanism of expression of long-term enhancement of hippocampal synapses: current issues and theoretical implications. Annu Rev Physiol. 1993;55:375–396. doi: 10.1146/annurev.ph.55.030193.002111. [DOI] [PubMed] [Google Scholar]
  18. Meister M., Pine J., Baylor D. A. Multi-neuronal signals from the retina: acquisition and analysis. J Neurosci Methods. 1994 Jan;51(1):95–106. doi: 10.1016/0165-0270(94)90030-2. [DOI] [PubMed] [Google Scholar]
  19. Meister M., Wong R. O., Baylor D. A., Shatz C. J. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science. 1991 May 17;252(5008):939–943. doi: 10.1126/science.2035024. [DOI] [PubMed] [Google Scholar]
  20. Otsu Y., Kimura F., Tsumoto T. Hebbian induction of LTP in visual cortex: perforated patch-clamp study in cultured neurons. J Neurophysiol. 1995 Dec;74(6):2437–2444. doi: 10.1152/jn.1995.74.6.2437. [DOI] [PubMed] [Google Scholar]
  21. Robinson H. P., Kawahara M., Jimbo Y., Torimitsu K., Kuroda Y., Kawana A. Periodic synchronized bursting and intracellular calcium transients elicited by low magnesium in cultured cortical neurons. J Neurophysiol. 1993 Oct;70(4):1606–1616. doi: 10.1152/jn.1993.70.4.1606. [DOI] [PubMed] [Google Scholar]
  22. Tsumoto T. Long-term potentiation and long-term depression in the neocortex. Prog Neurobiol. 1992 Aug;39(2):209–228. doi: 10.1016/0301-0082(92)90011-3. [DOI] [PubMed] [Google Scholar]
  23. Watanabe S., Jimbo Y., Kamioka H., Kirino Y., Kawana A. Development of low magnesium-induced spontaneous synchronized bursting and GABAergic modulation in cultured rat neocortical neurons. Neurosci Lett. 1996 May 24;210(1):41–44. doi: 10.1016/0304-3940(96)12653-7. [DOI] [PubMed] [Google Scholar]
  24. Wong R. O., Meister M., Shatz C. J. Transient period of correlated bursting activity during development of the mammalian retina. Neuron. 1993 Nov;11(5):923–938. doi: 10.1016/0896-6273(93)90122-8. [DOI] [PubMed] [Google Scholar]

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