Elsevier

Neuroscience

Volume 110, Issue 3, 20 March 2002, Pages 395-401
Neuroscience

Letter to Neuroscience
Properties and origin of spikelets in thalamocortical neurones in vitro

https://doi.org/10.1016/S0306-4522(01)00577-2Get rights and content

Abstract

Spikelets, or fast prepotentials as they are frequently referred to, are a common feature of the electrophysiology of central neurones and are invariably correlated with the presence of electrotonic coupling via gap junctions (Dudek et al., 1998, Perez Velazquez and Carlen, 2000). Here we report that in the presence of the metabotropic glutamate receptor agonists, trans-ACPD or DHPG, thalamocortical neurones of the cat dorsal lateral geniculate nucleus maintained in vitro exhibit stereotypical spikelets that possess similar properties to those described in other brain areas. These spikelets were routinely observed in the presence of antagonists of fast chemical synaptic transmission, were resistant to the application of a variety of voltage-dependent Ca2+ channel blockers but were abolished by tetrodotoxin. In addition, spikelets were reversibly blocked by the putative gap junction blocker carbenoxolone and were nearly always accompanied by dye-coupling. These results indicate that thalamocortical neurones may be electrotonically coupled via gap junctions with spikelets representing attenuated action potentials from adjoining cells. We suggest that the presence of electrotonic communication between thalamocortical neurones would have major implications for the understanding of both physiological (Steriade et al., 1993, Sillito et al., 1994, Alonso et al., 1996, Neuenschwander and Singer, 1996, Weliky and Katz, 1999) and pathological (Steriade and Contreras, 1995, Pinault et al., 1998) synchronised electrical activity in the thalamus.

Section snippets

Experimental procedures

All the procedures involving experimental animals were carried out in accordance with the UK Animals (Scientific Procedure) Act, 1986 and local ethics committee guidelines. All efforts were made to minimise animal suffering and the number of animals used. Young adult cats (1–1.5 kg) were deeply anaesthetised with a mixture of O2 and NO2 (2:1) and 1% halothane, a wide craniotomy performed and the brain removed. Coronal or sagittal slices of the thalamus containing the LGN were prepared and

Acknowledgements

We wish to thank Dr H.R. Parri for helpful discussion on the manuscript. We are grateful to Mr. T.M. Gould for excellent technical assistance. This work was supported by the Wellcome Trust (Grant 37089-98).

References (35)

  • L. Domich et al.

    Thalamic burst patterns in the naturally sleeping cat: a comparison between cortically projecting and reticularis neurones

    J. Physiol.

    (1986)
  • A. Draguhn et al.

    Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro

    Nature

    (1998)
  • M. Galarretta et al.

    A network of fast-spiking cells in the neocortex connected by electrical synapses

    Nature

    (1999)
  • J.R. Gibson et al.

    Two networks of electrically coupled inhibitory neurons in neocortex

    Nature

    (1999)
  • J.G. Jefferys

    Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions

    Physiol. Rev.

    (1995)
  • C.E. Landisman et al.

    Electrical synapses between thalamic reticular neurons

    Soc. Neurosci. Abstr.

    (2000)
  • A.R. Lieberman et al.

    Filamentous contacts: the ultrastructure and three-dimensional organization of specialized non-synaptic interneuronal appositions in thalamic relay nuclei

    Cell Tissue Res.

    (1997)
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    Present address: MRC Anatomical Neuropharmacology Unit, University Department of Pharmacology, University of Oxford, Mansfield Road, Oxford OX1 3TH, UK.

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