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The Journal of Neurophysiology Vol. 83 No. 5 May 2000, pp. 3084-3100
Copyright ©2000 by the American Physiological Society
1Cajal Neuroscience Center, Division of Life Sciences, University of Texas at San Antonio, San Antonio, Texas 78249; and 2Department of Anatomy and Neurobiology, University of Tennessee, Memphis, Tennessee 39163
Wilson, C. J. and
J. C. Callaway.
Coupled Oscillator Model of the Dopaminergic Neuron of the
Substantia Nigra. J. Neurophysiol. 83: 3084-3100, 2000. Calcium imaging using fura-2 and whole cell recording
revealed the effective location of the oscillator mechanism on
dopaminergic neurons of the substantia nigra, pars compacta, in slices
from rats aged 15-20 days. As previously reported, dopaminergic
neurons fired in a slow rhythmic single spiking pattern. The underlying membrane potential oscillation survived blockade of sodium currents with TTX and was enhanced by blockade of voltage-sensitive potassium currents with TEA. Calcium levels increased during the subthreshold depolarizing phase of the membrane potential oscillation and peaked at
the onset of the hyperpolarizing phase as expected if the pacemaker potential were due to a low-threshold calcium current and the hyperpolarizing phase to calcium-dependent potassium current. Calcium
oscillations were synchronous in the dendrites and soma and were
greater in the dendrites than in the soma. Average calcium levels in
the dendrites overshot steady-state levels and decayed over the course
of seconds after the oscillation was resumed after having been halted
by hyperpolarizing currents. Average calcium levels in the soma
increased slowly, taking many cycles to achieve steady state. Voltage
clamp with calcium imaging revealed the voltage dependence of the
somatic calcium current without the artifacts of incomplete spatial
voltage control. This showed that the calcium current had little or no
inactivation and was half-maximal at 
40 to 30 mV. The time constant
of calcium removal was measured by the return of calcium to resting
levels and depended on diameter. The calcium sensitivity of the
calcium-dependent potassium current was estimated by plotting the slow
tail current against calcium concentration during the decay of calcium
to resting levels at 60 mV. A single compartment model of the
dopaminergic neuron consisting of a noninactivating low-threshold
calcium current, a calcium-dependent potassium current, and a small
leak current reproduced most features of the membrane potential
oscillations. The same currents much more accurately reproduced the
calcium transients when distributed uniformly along a tapering cable in a multicompartment model. This model represented the dopaminergic neuron as a set of electrically coupled oscillators with different natural frequencies. Each frequency was determined by the surface area
to volume ratio of the compartment. This model could account for
additional features of the dopaminergic neurons seen in slices, such as
slow adaptation of oscillation frequency and may produce irregular
firing under different coupling conditions.
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