Journal of Neuroscience, Vol 6, 2298-2311, Copyright © 1986 by Society for Neuroscience
Integrative mechanisms controlling directional sensitivity of an identified sensory interneuron
GA Jacobs, JP Miller and RK Murphey
Several identified interneurons in the cricket cercal afferent system
display directional sensitivity to wind stimuli: the spike frequency of
these cells depends on the wind direction with respect to the animal's
body. Factors determining the directional sensitivity of one of these
identified interneurons (interneuron 10-3) were studied in detail. This
cell has 3 dendritic branches that arborize in 3 distinct regions of the
terminal abdominal ganglion. Using 2 independent methods, it was
demonstrated that the dendrites have different receptive fields to wind
stimuli. First, small patches of filiform hairs, whose afferents projected
to individual dendrites, were isolated and selectively stimulated. In each
case the response of the cell matched the receptive field of the afferents
in the patch. Second, a laser beam directed through the stereo dissecting
microscope was used to photoinactivate small portions of the cell in situ
during intracellular recording. By isolating or ablating individual
dendrites, the contributions of each of the 3 dendrites to the overall
receptive field were assessed. Although the receptive field of the whole
cell could be predicted by a summation of the receptive fields of all 3
dendrites, the precise directional sensitivity of the cell could not be
predicted by a simple linear summation of the receptive fields of each
dendrite. Two factors were found to account for this nonlinearity of
summation. The first factor was polysynaptic inhibition from other
interneurons within the terminal abdominal ganglion. Wind directions that
activate inhibition in interneuron 10-3 were identified, and the specific
classes of filiform afferents that activate the inhibitory pathway were
determined. The net effect of the inhibition was to "sharpen" the
directional sensitivity of 10-3 by selectively decreasing the cell's
response to specific excitatory inputs. The second factor that contributed
to directional sensitivity was the complex electroanatomy of the
interneuron. The probable location of the spike-initiating zone (SIZ) was
determined by using the laser photoinactivation technique. The relative
efficacies of synaptic inputs onto the 3 different branches were then
interpreted with respect to their different electrotonic distances from the
SIZ. On the basis of the data obtained in this report, we present a
qualitative model for the basis of directional sensitivity in this cell.
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