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A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro

  1. Mark O. Cunningham *,
  2. Miles A. Whittington * , †,
  3. Andrea Bibbig ‡,
  4. Anita Roopun *,
  5. Fiona E. N. LeBeau *,
  6. Angelika Vogt §,
  7. Hannah Monyer §,
  8. Eberhard H. Buhl * , , and
  9. Roger D. Traub ‡ , ∥
  1. *School of Biomedical Sciences, The Worsley Building, University of Leeds, Leeds LS2 9JT, United Kingdom; ‡Department of Physiology and Pharmacology, State University of New York Downstate Medical Center, 450 Clarkson Avenue, Box 31, Brooklyn, NY 11203; and §Department of Clinical Neurobiology, University Hospital of Neurology, Im Neuenheimer Feld 364, 69120 Heidelberg, Germany

  1. Communicated by Nancy J. Kopell, Boston University, Boston, MA, March 24, 2004 (received for review January 19, 2004)

Abstract

Basic cellular and network mechanisms underlying gamma frequency oscillations (30–80 Hz) have been well characterized in the hippocampus and associated structures. In these regions, gamma rhythms are seen as an emergent property of networks of principal cells and fast-spiking interneurons. In contrast, in the neocortex a number of elegant studies have shown that specific types of principal neuron exist that are capable of generating powerful gamma frequency outputs on the basis of their intrinsic conductances alone. These fast rhythmic bursting (FRB) neurons (sometimes referred to as “chattering” cells) are activated by sensory stimuli and generate multiple action potentials per gamma period. Here, we demonstrate that FRB neurons may function by providing a large-scale input to an axon plexus consisting of gap-junctionally connected axons from both FRB neurons and their anatomically similar counterparts regular spiking neurons. The resulting network gamma oscillation shares all of the properties of gamma oscillations generated in the hippocampus but with the additional critical dependence on multiple spiking in FRB cells.

Footnotes

  • ↵ Deceased January 18, 2003.

  • ↵ †To whom correspondence should be addressed for questions on electrophysiology. E-mail: m.a.whittington{at}leeds.ac.uk ∥To whom correspondence should be addressed. E-mail: roger.traub{at}downstate.edu.

  • Abbreviations: FRB, fast rhythmic bursting; FS, fast spiking; LTS, low-threshold spiking; RS, regular spiking; AMPA, α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid; GABAA, γ-aminobutyric acid type A; EPSP, excitatory postsynaptic potential.

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