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The Journal of Neurophysiology Vol. 84 No. 6 December 2000, pp. 2777-2785
Copyright ©2000 by the American Physiological Society
Department of Physiology and Cell Biology, University of Nevada School of Medicine, Reno, Nevada 89557-0046
Hillsley, K.,
J. L. Kenyon, and
T. K. Smith.
Ryanodine-Sensitive Stores Regulate the Excitability of AH
Neurons in the Myenteric Plexus of Guinea-Pig Ileum. J. Neurophysiol. 84: 2777-2785, 2000. Myenteric
afterhyperpolarizing (AH) neurons are primary afferent neurons
within the gastrointestinal tract. Stimulation of the intestinal mucosa
evokes action potentials (AP) that are followed by a slow
afterhyperpolarization (AHPslow) in the soma. The role of
intracellular Ca2+ ([Ca2+]i) and
ryanodine-sensitive Ca2+ stores in modulating the
electrical activity of myenteric AH neurons was investigated by
recording membrane potential and bis-fura-2 fluorescence from 34 AH
neurons. Mean resting [Ca2+]i was ~200 nM.
Depolarizing current pulses that elicited APs evoked
AHPslow and an increase in
[Ca2+]i, with similar time courses. The
amplitudes and durations of AHPslow and the
Ca2+ transient were proportional to the number of evoked
APs, with each AP increasing [Ca2+]i by ~50
nM. Ryanodine (10 µM) significantly reduced both the amplitude and
duration (by 60%) of the evoked Ca2+ transient and
AHPslow over the range of APs tested (1-15).
Calcium-induced calcium release (CICR) was graded and proportional to
the number of APs, with each AP triggering a rise in
[Ca2+]i of ~30 nM Ca2+ via
CICR. This indicates that CICR amplifies Ca2+ influx.
Similar changes in [Ca2+]i and
AHPslow were evoked by two APs in control and six APs in ryanodine. Thus, the magnitude of the change in bulk
[Ca2+]i and not the source of the
Ca2+ is the determinant of the magnitude of
AHPslow. Furthermore, lowering of free
[Ca2+]i, either by reducing extracellular
Ca2+ or injecting high concentrations of Ca2+
buffer, induced depolarization, increased excitability, and abolition of AHPslow. In addition, activation of synaptic input to AH
neurons elicited a slow excitatory postsynaptic potential (sEPSP) that was completely blocked in ryanodine. These results demonstrate the
importance of [Ca2+]i and CICR in sensory
processing in AH neurons. Activity-dependent CICR may be a mechanism to
grade the output of AH neurons according to the intensity of sensory input.
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