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Mechanoreceptors involved in the hindwing-evoked escape behaviour in cricket, Gryllus bimaculatus

Tetsutaro Hiraguchi^1,*, Tsuneo Yamaguchi² and Masakazu Takahata¹

¹ Division of Biological Sciences, Graduate School of Science, Hokkaido, University, Sapporo 060-0810, Japan
² Kawasaki College of Allied Health Professions, Kurashiki 701-0194, Japan

View larger version (58K): [in a new window]   Fig. 1. Morphology of the hindwing and vein diversion. (A) Dorsal view of the hindwing. The forewing was removed to expose the whole hindwing in its folded position. (B) Metathoracic ganglion and schematic diagram of the wing nerve branching pattern, showing nerve roots (R) and branched nerves (Br). (C) Schematic drawing of the hindwing extended. Veins are numbered successively from the most anterior (#1) to the most proximal (#10). The dark grey region corresponds to the portion indicated with an asterisk in A. The proximal part of the hindwing is covered by the forewing to the level of the 17th or 18th cell from the most distal cell (mean ± S.E.M. 17.7±0.2; N=5). The light grey region indicates the vannus region. The remaining part is called the remigium. (D) Optical microscopic view of the encircled part in C.

View larger version (33K): [in a new window]   Fig. 2. Functional region of the hindwing for detecting mechanical stimuli that elicit escape jumping. (A) Comparison of the occurrence probability of escape response to the pinching stimuli applied to the hindwing tip. There was no significant difference between intact animals and those animals with the hindwing immobilized (fixed). (B) Experimental setup for recording neural activities from the nerve branch supplying hindwing proprioceptors. Adapted from Kutsch and Huber (1989). A sample record is also shown. (C) Activities of proprioceptors recorded extracellularly. Left and right panels show activities in intact and fixed conditions, respectively. In each panel, the upper trace shows spontaneous activities, whereas the lower trace shows activities during pinching stimulation monitored by the bottom trace. (D) Schematic drawing of the branching pattern of veins #1-#10. Arrows indicate type I sensillae. The line widths indicate the relative thickness of each vein. The broken lines show thin cuticular layer parts in veins. The double lines show the cutting point for the experiment shown in E and lower case letters show experimental conditions. (E) Comparison of occurrence probability of escape response to the pinching stimuli in animals with the hindwing partially removed. A, the vannus removed; b, the vannus and veins #4, #5, #6 and #9 removed; c, veins #2, #3, #7, #8 and #10 removed.

View larger version (61K): [in a new window]   Fig. 3. Structure of mechanosensory hairs on the hindwing surface examined by a scanning electron microscope. (A,B) Type I sensillae. (C,D) Type III sensillae. (E) Histogram showing the length distribution of sensillae on the hindwing.

View larger version (64K): [in a new window]   Fig. 4. Structure of type II sensillae. (A) An arrowhead indicates the sensilla. The sensillae exist near the cross vein, which is swollen in the distal part of each cell. (B) The twisted hair shaft. Many grooves were seen on the surface. Distal is to the right, anterior to the top (A,B). (C) The hair shaft deflected towards the cuticular surface. Viewed from the distal direction. No pore was found on the tip of the shaft.

View larger version (19K): [in a new window]   Fig. 5. Number of sensory hairs on the dorso-distal part of the hindwing. Means ± S.E.M. are shown. (A) Type II hairs on each cell between veins #7 and #8. Cells are numbered successively from the most distal cell, #20 being the most proximal cell. (B) Type II hairs on veins #7 and #8. (C) Type I and type III hairs on veins #7 and #8. An arrowhead shows the cell to which the hindwing was covered by the distal part of the forewing.

View larger version (28K): [in a new window]   Fig. 8. Stimulation of type II sensory hairs on the distal part of cell series between veins #7 and #8 in the same preparation. Most units responded with one or a few spikes to a single stimulus. Distal is to the bottom, anterior to the right.

View larger version (48K): [in a new window]   Fig. 6. Conduction velocity of the hindwing mechanosensory signals. Two pairs of hook electrodes were placed on the wing nerve separated by 1.8 mm from each other. (A) Responses to stimulation of type I sensillae on the proximal part of the hindwing. To eliminate spontaneous spike activity of other units, the distal portion of the wing nerve was crushed. The upper (elec. 1) and lower (elec. 2) records were obtained by the distal and proximal electrode, respectively. The bottom trace monitored the stimulus. The lower panel is a partial expansion of the upper panel. (B) Responses to stimulation of type II sensillae on the distal part of the hindwing. The trace between the upper and lower panels is the high-gain reproduction of the record shown in the upper trace (elec. 1). (C) Responses to stimulation of campaniform sensillae on the proximal part. (D) Experimental setup and location of each type of sensillae stimulated in the experiment. (E) Conduction velocity of the sensory units associated with each type of sensillae. I, II and C indicate type I, II and campaniform sensillae, respectively.

View larger version (22K): [in a new window]   Fig. 7. Afferent responses to stimulation of a single type II sensilla. (A) The hair shaft was deflected toward the cuticular surface and returned to its original position with a tungsten stylus that was moved by a single cycle of sinusoidal function at varying frequencies (0.1 Hz, 1 Hz, 10 Hz and 100 Hz). Three representative records are shown for each frequency. The bottom trace monitors the stimulus. The rightmost panel shows the record when the cuticular surface in the vicinity of the deflected sensilla was stimulated to demonstrate that the observed response to 1-100 Hz stimulation was directly caused by shaft deflection. (B) The hair shaft was lifted up from the cuticular surface and returned to its original position. The polarity of the stimulus monitor (bottom trace) is reversed accordingly. Responses to stimulation at 1 Hz and 10 Hz are shown. (C) Number of elicited spikes for 10 stimulation trials plotted against stimulus frequency. The chart is based on the type II unit responses to lift-up stimulation exemplified in B.

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