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The Journal of Neuroscience, December 15, 2002, 22(24):10580-10592
Bursting in Leech Heart Interneurons: Cell-Autonomous and
Network-Based Mechanisms
Gennady S.
Cymbalyuk,
Quentin
Gaudry,
Mark A.
Masino, and
Ronald L.
Calabrese
Biology Department, Emory University, Atlanta, Georgia 30322
Rhythmic activity within the heartbeat pattern generator of the
medicinal leech is based on the alternating bursting of mutually inhibitory pairs of oscillator heart interneurons (half-center oscillators). Bicuculline methiodide has been shown to block mutual inhibition between these interneurons and to cause them to spike tonically while recorded intracellularly (Schmidt and Calabrese, 1992).
Using extracellular recording techniques, we show here that oscillator
and premotor heart interneurons continue to burst when
pharmacologically isolated with bicuculline, although the bursting is
not robust in some preparations. We propose that a nonspecific leak
current introduced by the intracellular microelectrode suppresses
endogenous bursting activity to account for the discrepancy with
results using intracellular recording. A two-parameter bifurcation diagram (Eleak vs
gleak) of a mathematical model of a
single heart interneuron shows a narrow stripe of parameter values
where bursting occurs, separating large zones of tonic spiking and
silence. A similar analysis performed for a half-center oscillator
model outlined a much larger area of bursting. Bursting in the
half-center oscillator model is also less sensitive to variation in the
maximal conductances of voltage-gated currents than in the
single-neuron model. Thus, in addition to ensuring appropriate bursting
characteristics such as period, phase, and duty cycles, the half-center
configuration enhances oscillation robustness, making them less
susceptible to random or imposed changes in membrane parameters.
Endogenous bursting, in turn, ensures appropriate bursting if the
strength of mutual inhibition is weakened and limits the minimum period of the half-center oscillator to a period near that of the single neuron.
Key words:
half-center oscillator; Hirudo medicinalis; bicuculline methiodide; dynamical system; bifurcation analysis; leak
current
Copyright © 2002 Society for Neuroscience 0270-6474/02/222410580-13$05.00/0
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