Multiple Conductances Cooperatively Regulate Spontaneous Bursting in Mouse Olfactory Bulb External Tufted Cells

J Neurosci. 2008 Feb 13;28(7):1625-39. doi: 10.1523/JNEUROSCI.3906-07.2008.

Abstract

External tufted (ET) cells are juxtaglomerular neurons that spontaneously generate bursts of action potentials, which persist when fast synaptic transmission is blocked. The intrinsic mechanism of this autonomous bursting is unknown. We identified a set of voltage-dependent conductances that cooperatively regulate spontaneous bursting: hyperpolarization-activated inward current (I(h)), persistent Na+ current (I(NaP)), low-voltage-activated calcium current (I(L/T)) mediated by T- and/or L-type Ca2+ channels, and large-conductance Ca2+-dependent K+ current (I(BK)). I(h) is important in setting membrane potential and depolarizes the cell toward the threshold of I(NaP) and I(T/L), which are essential to generate the depolarizing envelope that is crowned by a burst of action potentials. Action potentials depolarize the membrane and induce Ca2+ influx via high-voltage-activated Ca2+ channels (I(HVA)). The combined depolarization and increased intracellular Ca2+ activates I(BK), which terminates the burst by hyperpolarizing the membrane. Hyperpolarization activates I(h) and the cycle is regenerated. A novel finding is the role of L-type Ca2+ channels in autonomous ET cells bursting. A second novel feature is the role of BK channels, which regulate burst duration. I(L) and I(BK) may go hand-in-hand, the slow inactivation of I(L) requiring I(BK)-dependent hyperpolarization to deactivate inward conductances and terminate the burst. ET cells receive monosynaptic olfactory nerve input and drive the major inhibitory interneurons of the glomerular circuit. Modulation of the conductances identified here can regulate burst frequency, duration, and spikes per burst in ET cells and thus significantly shape the impact of glomerular circuits on mitral and tufted cells, the output channels of the olfactory bulb.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • Male
  • Membrane Potentials
  • Mice
  • Mice, Inbred C57BL
  • Neurons / metabolism*
  • Olfactory Bulb / cytology*
  • Patch-Clamp Techniques
  • Potassium Channels, Calcium-Activated / metabolism*
  • Sodium Channels / metabolism*

Substances

  • Potassium Channels, Calcium-Activated
  • Sodium Channels