Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1994 Nov 15;481(Pt 1):79–95. doi: 10.1113/jphysiol.1994.sp020420

A branching dendritic model of a rodent CA3 pyramidal neurone.

R D Traub 1, J G Jefferys 1, R Miles 1, M A Whittington 1, K Tóth 1
PMCID: PMC1155867  PMID: 7853251

Abstract

1. We constructed a branching dendritic compartmental model of a CA3 pyramidal neurone, using experimental data from guinea-pig and rat cells obtained in vitro. The goal was to understand interactions between synaptic events impinging on dendritic branches and voltage- and calcium-dependent currents. The model contained sixty-four soma-dendrite (SD) compartments, an axon initial segment (IS), and four axonal compartments. There were six active conductances in the SD membrane, including a sodium conductance (gNa) and a high-threshold calcium conductance (gCa), with kinetic properties similar to those reported in a previous study. 2. The distribution of conductance densities across the IS and SD was adjusted by testing the model response to antidromic stimulation and current pulses or sustained currents injected into the soma or apical dendrites. As before, gNa was concentrated on and near the soma with lower density in the dendrites, while gCa had a higher density in apical dendrites than at the soma. 3. The model predicts that CA3 pyramidal neurones in media blocking synaptic transmission should fire a burst of action potentials following antidromic stimulation. This was confirmed experimentally in hippocampal slices. 4. Both in the model and in guinea-pig neurones, dendritic IPSCs can delay the onset of bursting. If an IPSC begins soon enough after the first fast action potential, the later burst envelope is attenuated. This effect results from suppression of dendritic Ca2+ electrogenesis. 5. The model predicts that an appropriately timed dendritic IPSC (after the first somatic spike but before the dendritic Ca2+ spike) may suppress the transient local [Ca2+] signal, while having a negligible effect on the electrical output of the neurone. This phenomenon has been reported in guinea-pig Purkinje cells. 6. We conclude that active dendritic currents are critical for regulation of the electrical output of CA3 pyramidal neurones. We suggest also that dendritic [Ca2+] signals might be controlled in individual dendrites independently of action potential outputs, an effect of possible importance for synaptic plasticity.

Full text

PDF
79

Selected References

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

  1. Amitai Y., Friedman A., Connors B. W., Gutnick M. J. Regenerative activity in apical dendrites of pyramidal cells in neocortex. Cereb Cortex. 1993 Jan-Feb;3(1):26–38. doi: 10.1093/cercor/3.1.26. [DOI] [PubMed] [Google Scholar]
  2. Andersen P., Silfvenius H., Sundberg S. H., Sveen O., Wigström H. Functional characteristics of unmyelinated fibres in the hippocampal cortex. Brain Res. 1978 Apr 7;144(1):11–18. doi: 10.1016/0006-8993(78)90431-6. [DOI] [PubMed] [Google Scholar]
  3. Caeser M., Brown D. A., Gähwiler B. H., Knöpfel T. Characterization of a calcium-dependent current generating a slow afterdepolarization of CA3 pyramidal cells in rat hippocampal slice cultures. Eur J Neurosci. 1993 Jun 1;5(6):560–569. doi: 10.1111/j.1460-9568.1993.tb00521.x. [DOI] [PubMed] [Google Scholar]
  4. Gulyás A. I., Miles R., Hájos N., Freund T. F. Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur J Neurosci. 1993 Dec 1;5(12):1729–1751. doi: 10.1111/j.1460-9568.1993.tb00240.x. [DOI] [PubMed] [Google Scholar]
  5. Gulyás A. I., Miles R., Sík A., Tóth K., Tamamaki N., Freund T. F. Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature. 1993 Dec 16;366(6456):683–687. doi: 10.1038/366683a0. [DOI] [PubMed] [Google Scholar]
  6. Halliwell J. V., Adams P. R. Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res. 1982 Oct 28;250(1):71–92. doi: 10.1016/0006-8993(82)90954-4. [DOI] [PubMed] [Google Scholar]
  7. Hoehn K., Watson T. W., MacVicar B. A. A novel tetrodotoxin-insensitive, slow sodium current in striatal and hippocampal neurons. Neuron. 1993 Mar;10(3):543–552. doi: 10.1016/0896-6273(93)90341-n. [DOI] [PubMed] [Google Scholar]
  8. Ishizuka N., Weber J., Amaral D. G. Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol. 1990 May 22;295(4):580–623. doi: 10.1002/cne.902950407. [DOI] [PubMed] [Google Scholar]
  9. Jaffe D. B., Johnston D., Lasser-Ross N., Lisman J. E., Miyakawa H., Ross W. N. The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons. Nature. 1992 May 21;357(6375):244–246. doi: 10.1038/357244a0. [DOI] [PubMed] [Google Scholar]
  10. KANDEL E. R., SPENCER W. A., BRINLEY F. J., Jr Electrophysiology of hippocampal neurons. I. Sequential invasion and synaptic organization. J Neurophysiol. 1961 May;24:225–242. doi: 10.1152/jn.1961.24.3.225. [DOI] [PubMed] [Google Scholar]
  11. Kay A. R., Wong R. K. Calcium current activation kinetics in isolated pyramidal neurones of the Ca1 region of the mature guinea-pig hippocampus. J Physiol. 1987 Nov;392:603–616. doi: 10.1113/jphysiol.1987.sp016799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Knöpfel T., Gähwiler B. H. Activity-induced elevations of intracellular calcium concentration in pyramidal and nonpyramidal cells of the CA3 region of rat hippocampal slice cultures. J Neurophysiol. 1992 Sep;68(3):961–963. doi: 10.1152/jn.1992.68.3.961. [DOI] [PubMed] [Google Scholar]
  13. Kocsis J. D., Waxman S. G. Absence of potassium conductance in central myelinated axons. Nature. 1980 Sep 25;287(5780):348–349. doi: 10.1038/287348a0. [DOI] [PubMed] [Google Scholar]
  14. Kosaka T. The axon initial segment as a synaptic site: ultrastructure and synaptology of the initial segment of the pyramidal cell in the rat hippocampus (CA3 region). J Neurocytol. 1980 Dec;9(6):861–882. doi: 10.1007/BF01205024. [DOI] [PubMed] [Google Scholar]
  15. Kullmann D. M., Perkel D. J., Manabe T., Nicoll R. A. Ca2+ entry via postsynaptic voltage-sensitive Ca2+ channels can transiently potentiate excitatory synaptic transmission in the hippocampus. Neuron. 1992 Dec;9(6):1175–1183. doi: 10.1016/0896-6273(92)90075-o. [DOI] [PubMed] [Google Scholar]
  16. Llinas R., Nicholson C. Electrophysiological properties of dendrites and somata in alligator Purkinje cells. J Neurophysiol. 1971 Jul;34(4):532–551. doi: 10.1152/jn.1971.34.4.532. [DOI] [PubMed] [Google Scholar]
  17. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol. 1980 Aug;305:197–213. doi: 10.1113/jphysiol.1980.sp013358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Maccaferri G., Mangoni M., Lazzari A., DiFrancesco D. Properties of the hyperpolarization-activated current in rat hippocampal CA1 pyramidal cells. J Neurophysiol. 1993 Jun;69(6):2129–2136. doi: 10.1152/jn.1993.69.6.2129. [DOI] [PubMed] [Google Scholar]
  19. Masukawa L. M., Prince D. A. Synaptic control of excitability in isolated dendrites of hippocampal neurons. J Neurosci. 1984 Jan;4(1):217–227. doi: 10.1523/JNEUROSCI.04-01-00217.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. McCormick D. A., Huguenard J. R. A model of the electrophysiological properties of thalamocortical relay neurons. J Neurophysiol. 1992 Oct;68(4):1384–1400. doi: 10.1152/jn.1992.68.4.1384. [DOI] [PubMed] [Google Scholar]
  21. Midtgaard J. Stellate cell inhibition of Purkinje cells in the turtle cerebellum in vitro. J Physiol. 1992 Nov;457:355–367. doi: 10.1113/jphysiol.1992.sp019382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Miles R. Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig in vitro. J Physiol. 1990 Sep;428:61–77. doi: 10.1113/jphysiol.1990.sp018200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Miles R., Traub R. D., Wong R. K. Spread of synchronous firing in longitudinal slices from the CA3 region of the hippocampus. J Neurophysiol. 1988 Oct;60(4):1481–1496. doi: 10.1152/jn.1988.60.4.1481. [DOI] [PubMed] [Google Scholar]
  24. Miles R., Wong R. K. Excitatory synaptic interactions between CA3 neurones in the guinea-pig hippocampus. J Physiol. 1986 Apr;373:397–418. doi: 10.1113/jphysiol.1986.sp016055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Miles R., Wong R. K. Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J Physiol. 1987 Jul;388:611–629. doi: 10.1113/jphysiol.1987.sp016634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miles R., Wong R. K. Unitary inhibitory synaptic potentials in the guinea-pig hippocampus in vitro. J Physiol. 1984 Nov;356:97–113. doi: 10.1113/jphysiol.1984.sp015455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Miyakawa H., Lev-Ram V., Lasser-Ross N., Ross W. N. Calcium transients evoked by climbing fiber and parallel fiber synaptic inputs in guinea pig cerebellar Purkinje neurons. J Neurophysiol. 1992 Oct;68(4):1178–1189. doi: 10.1152/jn.1992.68.4.1178. [DOI] [PubMed] [Google Scholar]
  28. Miyakawa H., Ross W. N., Jaffe D., Callaway J. C., Lasser-Ross N., Lisman J. E., Johnston D. Synaptically activated increases in Ca2+ concentration in hippocampal CA1 pyramidal cells are primarily due to voltage-gated Ca2+ channels. Neuron. 1992 Dec;9(6):1163–1173. doi: 10.1016/0896-6273(92)90074-n. [DOI] [PubMed] [Google Scholar]
  29. Numann R. E., Wadman W. J., Wong R. K. Outward currents of single hippocampal cells obtained from the adult guinea-pig. J Physiol. 1987 Dec;393:331–353. doi: 10.1113/jphysiol.1987.sp016826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Otis T. S., De Koninck Y., Mody I. Characterization of synaptically elicited GABAB responses using patch-clamp recordings in rat hippocampal slices. J Physiol. 1993 Apr;463:391–407. doi: 10.1113/jphysiol.1993.sp019600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pearce R. A. Physiological evidence for two distinct GABAA responses in rat hippocampus. Neuron. 1993 Feb;10(2):189–200. doi: 10.1016/0896-6273(93)90310-n. [DOI] [PubMed] [Google Scholar]
  32. Schwartzkroin P. A. Further characteristics of hippocampal CA1 cells in vitro. Brain Res. 1977 Jun 3;128(1):53–68. doi: 10.1016/0006-8993(77)90235-9. [DOI] [PubMed] [Google Scholar]
  33. Somogyi P., Nunzi M. G., Gorio A., Smith A. D. A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells. Brain Res. 1983 Jan 17;259(1):137–142. doi: 10.1016/0006-8993(83)91076-4. [DOI] [PubMed] [Google Scholar]
  34. Storm J. F. Temporal integration by a slowly inactivating K+ current in hippocampal neurons. Nature. 1988 Nov 24;336(6197):379–381. doi: 10.1038/336379a0. [DOI] [PubMed] [Google Scholar]
  35. Thompson S. M., Wong R. K. Development of calcium current subtypes in isolated rat hippocampal pyramidal cells. J Physiol. 1991 Aug;439:671–689. doi: 10.1113/jphysiol.1991.sp018687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Traub R. D., Miles R., Jefferys J. G. Synaptic and intrinsic conductances shape picrotoxin-induced synchronized after-discharges in the guinea-pig hippocampal slice. J Physiol. 1993 Feb;461:525–547. doi: 10.1113/jphysiol.1993.sp019527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Traub R. D., Wong R. K., Miles R., Michelson H. A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. J Neurophysiol. 1991 Aug;66(2):635–650. doi: 10.1152/jn.1991.66.2.635. [DOI] [PubMed] [Google Scholar]
  38. Turner R. W., Meyers D. E., Richardson T. L., Barker J. L. The site for initiation of action potential discharge over the somatodendritic axis of rat hippocampal CA1 pyramidal neurons. J Neurosci. 1991 Jul;11(7):2270–2280. doi: 10.1523/JNEUROSCI.11-07-02270.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Westenbroek R. E., Merrick D. K., Catterall W. A. Differential subcellular localization of the RI and RII Na+ channel subtypes in central neurons. Neuron. 1989 Dec;3(6):695–704. doi: 10.1016/0896-6273(89)90238-9. [DOI] [PubMed] [Google Scholar]
  40. Wong R. K., Prince D. A. Afterpotential generation in hippocampal pyramidal cells. J Neurophysiol. 1981 Jan;45(1):86–97. doi: 10.1152/jn.1981.45.1.86. [DOI] [PubMed] [Google Scholar]
  41. Wong R. K., Prince D. A., Basbaum A. I. Intradendritic recordings from hippocampal neurons. Proc Natl Acad Sci U S A. 1979 Feb;76(2):986–990. doi: 10.1073/pnas.76.2.986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wong R. K., Stewart M. Different firing patterns generated in dendrites and somata of CA1 pyramidal neurones in guinea-pig hippocampus. J Physiol. 1992 Nov;457:675–687. doi: 10.1113/jphysiol.1992.sp019401. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES