Brain Cell Biology

, Volume 35, Issue 1, pp 13–27 | Cite as

Electrical coupling between pyramidal cells in adult cortical regions

  • Audrey Mercer
  • A. Peter Bannister
  • Alex M. Thomson
Research Article


Recently, intense interest has focussed on electrical coupling between interneurones in cortical regions and their contributions towards oscillatory network activity. Despite mounting circumstantial evidence that pyramidal cells are also coupled, the paucity of direct evidence has made this controversial. Dual intracellular recordings from pairs of cortical and hippocampal pyramids demonstrated strong, but sparse coupling. Approximately 70% of CA1 pyramids close to the stratum radiatum border were coupled to another pyramid, but only to one or two of their very closest neighbours. On average 25% of the steady state and 10% of the peak action potential voltage change in one cell transferred to the other, supporting synchrony and promoting burst firing. The very high incidence of convergent inputs from coupled pyramids onto single targets provided additional evidence that ‘spikelets’ reflected full action potentials in a coupled cell, since the EPSPs activated by APs and by ‘spikelets’ had significantly different amplitude distributions.


Pyramidal Cell Electrical Coupling Carbenoxolone Coupling Ratio Biocytin 
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  1. Ali, A. B., Deuchars, J., Pawelzik, H., and Thomson, A. M. (1998). CA1 pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices. J. Physiol. 507, 201–217.PubMedCrossRefGoogle Scholar
  2. Baimbridge, K. G., Peet, M. J., McLennan, H., and Church, J. (1991). Bursting response to current- evoked depolarization in rat CA1 pyramidal neurons is correlated with lucifer yellow dye coupling but not with the presence of calbindin-D28k. Synapse 7, 269–277.PubMedCrossRefGoogle Scholar
  3. Beierlein, M., Gibson, J. R., and Connors, B. W. (2000). A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat. Neurosci. 3, 904–910.PubMedCrossRefGoogle Scholar
  4. Beierlein, M., Gibson, J. R., and Connors, B. W. (2003). Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J. Neurophysiol. 90, 2987–3000PubMedCrossRefGoogle Scholar
  5. Bruzzone, R., Barbe, M. T., Jakob, N. J., and Monyer, H. (2005). Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J. Neurochem. 92, 1033–1043.PubMedCrossRefGoogle Scholar
  6. Church, J. and Baimbridge, K. G. (1991). Exposure to high-pH medium increases the incidence and extent of dye coupling between rat hippocampal CA1 pyramidal neurons in vitro. J. Neurosci. 11, 3289–3295PubMedGoogle Scholar
  7. Deuchars, J. and Thomson, A. M. (1996). CA1 pyramid-pyramid connections in rat hippocampus in vitro: dual intracellular recordings with biocytin filling. Neuroscience 74, 1009–1018PubMedGoogle Scholar
  8. Deans, M. R., Gibson, J. R., Sellitto, C., Connors, B. W., and Paul, D. L. (2001). Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 31, 477–485.PubMedCrossRefGoogle Scholar
  9. Draguhn, A. Traub, R. D., Schmitz, D. and Jefferys, J. G. R. (1998). Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394, 189–192PubMedCrossRefGoogle Scholar
  10. Galarreta, M. and Hestrin, S. (2002). Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex. Proc. Natl. Acad. Sci. U.S.A. 99, 12438–12443PubMedCrossRefGoogle Scholar
  11. Galarreta, M., Erdelyi, F., Szabo, G., and Hestrin, S. (2004). Electrical coupling among irregular- spiking GABAergic interneurons expressing cannabinoid receptors. J. Neurosci. 24, 9770–9778.PubMedCrossRefGoogle Scholar
  12. Gibson, J. R., Beierlein, M., Connors, B. W. (1999). Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75–79.PubMedCrossRefGoogle Scholar
  13. Gibson, J. R., Beierlein, M., and Connors, B. W. (2005). Functional properties of electrical synapses between inhibitory interneurons of neocortical layer 4. J. Neurophysiol. 93, 467–480.PubMedCrossRefGoogle Scholar
  14. Gutnick, M. J. and Prince, D. A. (1981). Dye coupling and possible electrotonic coupling in the guinea pig neocortical slice. Science 21, 67–70CrossRefGoogle Scholar
  15. Hamzel-Sichani, F., Janssen, W. G., Hof, P. R., Wearne, S. L., Stewart, M. G., Whittington, M. A., and Traub, R. D. (2006). Gap junctions couple hippocampal mossy fiber axons to each other and to CA3 pyramidal cell dendrites. Abstract Viewer and Itinerary Planner. Washington, DC: Society for Neuroscience, 2006. 132.9 OnlineGoogle Scholar
  16. Hormuzdi, S. G., Pais, I., LeBeau, F. E., Towers, S. K., Rozov, A., Buhl, E. H., Whittington, M. A., and Monyer, H. (2001). Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 31, 487–495PubMedCrossRefGoogle Scholar
  17. Hughes, D. I., Bannister, A. P., Pawelzik, H., and Thomson, A. M. (2000). Double immuno-fluorescence, peroxidase labelling and ultrastructural analysis of interneurones following prolonged electrophysiological recordings in vitro. J. Neurosci. Meth. 101, 107–116.CrossRefGoogle Scholar
  18. Long, M. A., Cruikshank, S. J., Jutras, M. J., and Connors, B. W. (2005). Abrupt maturation of a spike-synchronizing mechanism in neocortex. J. Neurosci. 25, 7309–7316.PubMedCrossRefGoogle Scholar
  19. MacVicar, B. A. and Dudek, F. E. (1981). Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science 213, 782–785.PubMedCrossRefGoogle Scholar
  20. MacVicar, B. A. and Dudek, F. E. (1980). Dye-coupling between CA3 pyramidal cells in slices of rat hippocampus. Brain Res. 196, 494–497.PubMedCrossRefGoogle Scholar
  21. MacVicar, B. A., Ropert, N., and Krnjevic, K. (1982). Dye-coupling between pyramidal cells of rat hippocampus in vivo. Brain Res. 238, 239–244.PubMedCrossRefGoogle Scholar
  22. Nagy, J. I., Dudek, F. E., Rash, J. E. (2004). Update on connexins and gap junctions in neurons and glia in the mammalian nervous system. Brain. Res. Brain Res. Rev. 47, 191–215.PubMedCrossRefGoogle Scholar
  23. Pawelzik, H., Hughes, D. I., and Thomson, A. M. (2002). Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus. J. Comp. Neurol. 443, 346–67.PubMedCrossRefGoogle Scholar
  24. Schmitz, D., Schuchmann, S., Fisahn, A., Draguhn, A., Buhl, E. H., Petrasch-Parwez, E., Dermietzel, R., Heinemann, U., Traub, R. D. (2001). Axo-axonal coupling: a novel mechanism for ultrafast neuronal communication. Neuron 31, 831–840.PubMedCrossRefGoogle Scholar
  25. Simon, A., Olah, S., Molnar, G., Szabadics, J., and Tamas, G. (2005). Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J. Neurosci. 25, 6278–6285.PubMedCrossRefGoogle Scholar
  26. Tamas, G., Buhl, E. H., Lorincz, A., and Somogy, I. P. (2000). Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci. 3, 366–371.PubMedCrossRefGoogle Scholar
  27. Thomson, A. M. and Bannister, A. P. (2004). Electrical gap junctions involving somata and axons of neocortical and hippocampal pyramidal cells 403.13 2004. Abstract Viewer and Itinerary Planner. Washington, DC: Society for Neuroscience (Online).Google Scholar
  28. Thomson, A. M. and Radpour, S. (1991). Excitatory connections between CA1 pyramidal cells revealed by spike triggered averaging in slices of rat hippocampus are partially NMDA receptor mediated. Europ. J. Neurosci. 3, 587–601CrossRefGoogle Scholar
  29. Thomson, A. M. and West, D. C. (2003). Presynaptic frequency filtering in the gamma frequency band; dual intracellular recordings in slices of adult rat and cat neocortex Cereb. Cortex 13, 136–143.CrossRefGoogle Scholar
  30. Vogt, A., Hormuzdi, S. G., and Monyer, H. (2005). Pannexin1 and Pannexin2 expression in the developing and mature rat brain. Brain Res. Mol. Brain Res. 141, 113–120.PubMedCrossRefGoogle Scholar
  31. West, D. C., Mercer, A., Kirchhecker, S., Morris, O. T., and Thomson, A. M. (2006). Layer 6 cortico- thalamic pyramidal cells preferentially innervate interneurons and generate facilitating EPSPs. Cereb. Cortex 16, 200–211.PubMedCrossRefGoogle Scholar
  32. Zsiros, V. and Maccaferri, G. (2005). Electrical coupling between interneurons with different excitable properties in the stratum lacunosum-moleculare of the juvenile CA1 rat hippocampus. J. Neurosci. 25, 8686–8695.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2006

Authors and Affiliations

  • Audrey Mercer
    • 1
  • A. Peter Bannister
    • 1
    • 2
  • Alex M. Thomson
    • 1
  1. 1.Department of Pharmacology, The School of PharmacyLondon UniversityLondonU.K.
  2. 2.Thrombosis Research Institute, HistopathologyEmmanuel Kaye BuildingLondonU.K.

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