1. Six different types of primary wind-sensitive interneurons in the cricket cercal sensory system were tested for their sensitivity to the orientation and peak velocity of unidirectional airflow stimuli. 2. The cells could be grouped into two distinct classes on the basis of their thresholds and static sensitivities to airflow velocity. 3. Four interneurons (the right and left 10-2 cells and the right and left 10-3 cells) made up one of the two distinct velocity sensitivity classes. The mean firing frequencies of these interneurons were proportional to the logarithm of peak stimulus velocity over the range from 0.02 to 2.0 cm/s. 4. The other two interneurons studied (left and right 9-3) had a higher air-current velocity threshold, near the saturation level of the 10-2 and 10-3 interneurons. The slope of the velocity sensitivity curve for the 9-3 interneurons was slightly greater than that for the 10-2 and 10-3 interneurons, extending the sensitivity range of the system as a whole to at least 100 cm/s. 5. All of the interneurons had broad, symmetrical, single-lobed directional sensitivity tuning curves that could be accurately represented as truncated sine waves with 360 degree period. 6. The four low-threshold interneurons (i.e., left and right 10-2 and 10-3) had peak directional sensitivities that were evenly spaced around the horizontal plane, and their overlapping tuning curves covered all possible air-current stimulus orientations. The variance in the cells' responses to identical repeated stimuli varied between approximately 10% at the optimal stimulus orientations and approximately 30% at the zero-crossing orientations. 7. The two higher threshold interneurons (left and right 9-3) had broader directional sensitivity curves and wider spacing, resulting in reduced overlap with respect to the low-threshold class.
Several identified interneurons in the cricket cereal 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 spikeinitiating 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.The relationship between the structural and functional properties of neurons has long interested theoretical and experimental neurobiologists. In very few instances, however, has it been possible to test directly how the distribution of excitatory and inhibitory inputs to different dendritic regions of a cell results in an integrated output that is relevant to the behavior of the animal. These anatomical relationships are of special interest
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