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The Journal of Neurophysiology Vol. 84 No. 3 September 2000, pp. 1519-1530
Copyright ©2000 by the American Physiological Society
Department of Cell Biology and Anatomy, Neuroscience Research Group, University of Calgary, Calgary, Alberta T2N 4N1, Canada
Lemon, N. and
R. W. Turner.
Conditional Spike Backpropagation Generates Burst Discharge in a
Sensory Neuron. J. Neurophysiol. 84: 1519-1530, 2000. Backpropagating dendritic Na+
spikes generate a depolarizing afterpotential (DAP) at the soma of
pyramidal cells in the electrosensory lateral line lobe (ELL) of weakly
electric fish. Repetitive spike discharge is associated with a
progressive depolarizing shift in somatic spike afterpotentials that
eventually triggers a high-frequency spike doublet and subsequent burst
afterhyperpolarization (bAHP). The rhythmic generation of a spike
doublet and bAHP groups spike discharge into an oscillatory burst
pattern. This study examined the soma-dendritic mechanisms controlling
the depolarizing shift in somatic spike afterpotentials, and the
mechanism by which spike doublets terminate spike discharge.
Intracellular recordings were obtained from ELL pyramidal somata and
apical dendrites in an in vitro slice preparation. The pattern of spike
discharge was equivalent in somatic and dendritic regions, reflecting
the backpropagation of spikes from soma to dendrites. There was a clear
frequency-dependent threshold in the transition from tonic to burst
discharge, with bursts initiated when interspike intervals fell between
~3-7 ms. Removal of all backpropagating spikes by dendritic TTX
ejection revealed that the isolated somatic AHPs were entirely stable
at the interspike intervals that generated burst discharge. As such, the depolarizing membrane potential shift during repetitive discharge could be attributed to a potentiation of DAP amplitude. Potentiation of
the DAP was due to a frequency-dependent broadening and temporal summation of backpropagating dendritic Na+ spikes. Spike
doublets were generated with an interspike interval close to, but not
within, the somatic spike refractory period. In contrast, the
interspike interval of spike doublets always fell within the longer
dendritic refractory period, preventing backpropagation of the second
spike of the doublet. The dendritic depolarization was thus abruptly
removed from one spike to the next, allowing the burst to terminate
when the bAHP hyperpolarized the membrane. The transition from tonic to
burst discharge was dependent on the number and frequency of spikes
invoking dendritic spike summation, indicating that burst threshold
depends on the immediate history of cell discharge. Spike frequency
thus represents an important condition that determines the success of
dendritic spike invasion, establishing an intrinsic mechanism by which
backpropagating spikes can be used to generate a rhythmic burst output.
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