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The Journal of Neurophysiology Vol. 88 No. 1 July 2002, pp. 64-85
Copyright ©2002 by the American Physiological Society
Monell Chemical Senses Center, Philadelphia, Pennsylvania 19104-3308
Lowe, Graeme
Inhibition of Backpropagating Action Potentials in Mitral Cell
Secondary Dendrites. J. Neurophysiol. 88: 64-85, 2002. The mammalian olfactory bulb is a
geometrically organized signal-processing array that utilizes lateral
inhibitory circuits to transform spatially patterned inputs. A major
part of the lateral circuitry consists of extensively radiating
secondary dendrites of mitral cells. These dendrites are bidirectional
cables: they convey granule cell inhibitory input to the mitral soma,
and they conduct backpropagating action potentials that trigger
glutamate release at dendrodendritic synapses. This study examined how
mitral cell firing is affected by inhibitory inputs at different
distances along the secondary dendrite and what happens to
backpropagating action potentials when they encounter inhibition. These
are key questions for understanding the range and spatial dependence of lateral signaling between mitral cells. Backpropagating action potentials were monitored in vitro by simultaneous somatic and dendritic whole cell recording from individual mitral cells in rat
olfactory bulb slices, and inhibition was applied focally to dendrites
by laser flash photolysis of caged GABA (2.5-µm spot). Photolysis was
calibrated to activate conductances similar in magnitude to
GABAA-mediated inhibition from granule cell
spines. Under somatic voltage-clamp with CsCl dialysis, uncaging GABA onto the soma, axon initial segment, primary and secondary dendrites evoked bicuculline-sensitive currents (up to 
1.4 nA at 60 mV; reversal at ~0 mV). The currents exhibited a patchy distribution along the axon and dendrites. In current-clamp recordings, repetitive firing driven by somatic current injection was blocked by uncaging GABA
on the secondary dendrite ~140 µm from the soma, and the blocking
distance decreased with increasing current. In the secondary dendrites,
backpropagated action potentials were measured 93-152 µm from the
soma, where they were attenuated by a factor of 0.75 ± 0.07 (mean ± SD) and slightly broadened (1.19 ± 0.10),
independent of activity (35-107 Hz). Uncaging GABA on the distal
dendrite had little effect on somatic spikes but attenuated
backpropagating action potentials by a factor of 0.68 ± 0.15 (0.45-0.60 µJ flash with 1-mM caged GABA); attenuation was localized
to a zone of width 16.3 ± 4.2 µm around the point of GABA
release. These results reveal the contrasting actions of inhibition at
different locations along the dendrite: proximal inhibition blocks
firing by shunting somatic current, whereas distal inhibition can
impose spatial patterns of dendrodendritic transmission by locally
attenuating backpropagating action potentials. The secondary dendrites
are designed with a high safety factor for backpropagation, to
facilitate reliable transmission of the outgoing spike-coded data
stream, in parallel with the integration of inhibitory inputs.
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