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The Journal of Neuroscience, November 15, 2000, 20(22):8493-8503
Intrinsic Membrane Properties Underlying Spontaneous Tonic Firing in Neostriatal Cholinergic Interneurons
Ben D. Bennett1, Joseph C. Callaway2, and Charles J. Wilson1 1 Cajal Neuroscience Research Center, Division of Life Sciences, University of Texas, San Antonio, Texas 78249 and 2 Department of Anatomy and Neurobiology, University of Tennessee, Memphis, Tennesse 38163
Neostriatal cholinergic interneurons produce spontaneous tonic firing in the absence of synaptic input. Perforated patch recording and whole-cell recording combined with calcium imaging were used in vitro to identify the intrinsic membrane properties underlying endogenous excitability. Spontaneous firing was driven by the combined action of a sodium current and the hyperpolarization-activated cation current (Ih), which together ensured that there was no zero current point in the subthreshold voltage range. Blockade of sodium channels or Ih established a stable subthreshold resting membrane potential. A tetrodotoxin-sensitive region of negative slope conductance was observed between approximately
60 mV and threshold (approximately
Calcium imaging experiments revealed that there was minimal calcium influx at subthreshold membrane potentials but that action potentials produced elevations of calcium in both the soma and dendrites. Spike-triggered calcium entry shaped the falling phase of the action potential waveform and activated calcium-dependent potassium channels. Blockade of big-conductance channels caused spike broadening. Application of apamin, which blocks small-conductance channels, abolished the slow spike afterhyperpolarization (AHP) and caused a transition to burst firing.
In the absence of synaptic input, a range of tonic firing patterns are observed, suggesting that the characteristic spike sequences described for tonically active cholinergic neurons (TANs) recorded in vivo are intrinsic in origin. The pivotal role of the AHP in regulating spike patterning indicates that burst firing of TANs in vivo could arise from direct or indirect modulation of the AHP without requiring phasic synaptic input.
Key words: TANs; tonic firing; rhythmic bursting; spike sequences; irregular firing; sodium current; Ih
Copyright © 2000 Society for Neuroscience 0270-6474/00/20228493-11$05.00/0
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