Masamichi Kanou

The Air-puff Evoked Escape Behavior of the Cricket Gryllus bimaculatus and its Compensational Recovery after Cercal Ablations

Abstract The air-puff evoked escape behavior of the cricket, Gryllus bimaculatus, was investigated. Crickets almost always escaped away from the stimulus source. In an optimal condition, the mean escape direction was 162° opposite to the stimulus source. Stronger (higher velocity) air-puff elicited an escape in larger number of crickets. However, the escape direction became incorrect when the stimulus was too strong. Crickets with bilateral cercal ablation did not show any escape to an air-puff, while unilaterally ablated ones did respond to the same stimulus with an escape. However, the response rate of animals with unilateral cercal ablation was lower than that in intact animals. Although the mean escape direction of the crickets with unilateral cercal ablation was still opposite to the stimulus source, the direction was not so accurate as in intact animals. About 6 days after the unilateral cercal ablation, the response rate showed a statistically significant compensational recovery. On the other hand, 14 days were necessary for the recovery of the escape direction. Information which regulating the response rate and the behavioral orientation is likely being processed in different neural pathways.

Ecdysial growth of the filiform hairs and sensitivity of the cercal sensory system of the cricket,Gryllus bimaculatus

Summary1.The ecdysial growth of cercal filiform hairs was investigated in the cricketGryllus bimaculatus. The length of hairs varied from 40 to 500 μm in the 1st, from 40 to 650 μm in the 3rd and from 30 to 800 μm in the 5th instar nymphs (Fig. 1). Hemimetabolous development causes both hair growth and the appearance of new hairs at each ecdysis (Figs. 2, 3). The newly acquired hairs were shorter than 200 μm in every case (Fig. 4).2.Velocity thresholds of cercal sensory interneurons (CSIs) to sinusoidal air-currents were measured in 3rd instar nymphs (Fig. 5 A, B, C). CSIs 8-1 (medial giant interneuron: MGI) and 9-1 (lateral giant interneuron: LGI) showed threshold curves of acceleration sensitivity similar to those in adults. The thresholds for CSIs 8-1 and 9-1 were on the average higher in nymphs than in adults. The threshold curves for the two velocity-sensitive CSIs 10-2 and 10-3 were similar for nymphs and adults.3.Velocity thresholds of cercal filiform sensilla were measured in 3rd instar nymphs (Fig. 6). In spite of the small size of nymphal hairs, the most sensitive ones showed the same sensitivity as did the long 1000 μm hairs of the adult.4.The filiform hairs in 3rd instar nymphs were supported by a weaker spring than in adults (Fig. 7). Relative stiffness was about 50% of that in the long hairs in adults, but not much different than that in the short hairs.5.Based on a theoretical estimation of hair motion, the threshold angle of a filiform sensillum in the 3rd instar nymph was calculated (Fig. 9). Threshold angles of the long sensilla seemed to be unchanged throughout hemimetabolous development.

Directionality of Cricket Giant Interneurons to Escape Eliciting Unidirectional Air-Current

Abstract Response properties of six giant interneurons (GIs) 8-1, 9-1, 9-2, 9-3, 10-2 and 10-3 of the cricket, Gryllus bimaculatus, were investigated with a short duration unidirectional air-current stimulus which elicits escape behavior of the insects effectively. Air-currents were presented to the insects from 12 different directions in the horizontal plane in order to explore the directional characteristics of the GIs. The frequency dependency of velocity thresholds (threshold curves) of the GIs changed with the direction of stimulus air-current. Preferential directions of the GIs to the air-currents were ipsilateral-rear in Gl 8-1, ipsilateral-front in Gl 9-1, ipsilateral-rear in Gl 9-2, ipsilateral-front in Gl 9-3, ipsilateral-rear in Gl 10-2 and ipsilateral-front in Gl 10-3, with respect to the ventral nerve cord containing the axons. Intensity-response curves suggest that GIs 8-1 and 9-1 show the maximum response to air-current velocities lower than 300 mm/sec regardless of the stimulus direction. On the other hand, response magnitudes of GIs 9-2 and 9-3 increased proportional to the logarithm of the stimulus velocity up to 300 mm/sec and did not show a plateau even at 300 mm/sec regardless of the stimulus direction. Based on the directional characteristics revealed in the present study, a possible neural mechanism for encoding the direction of air-current by the combinational activity of GIs 9-2 and 9-3 is discussed.

Rearing conditions required for behavioral compensation after unilateral cercal ablation in the cricket Gryllus bimaculatus.

Abstract The rearing condition necessary for behavioral compensation after sensory deprivation was investigated in the cricket Gryllus bimaculatus. The right-cercus-ablated cricket was reared in a glass vial with a slightly larger diameter than the body length of the cricket. After two weeks of rearing in the vial, the air-puff-evoked escape behavior of the cricket was investigated. The response rate (relative occurrence of the escape behavior after a standard air puff) obtained was identical with that of crickets reared in a large cage. On the other hand, unlike crickets reared in a large cage, the distorted escape directional property of the cricket reared in the vial was not compensated at all. Control experiments proved that the restraint in the vial did not affect the motor system, and the air motion from environments was not essential for the compensational recovery of the escape direction. Therefore, the ablated crickets required spontaneous walking in order to compensate the directionality of their escape. A self-generated wind caused by spontaneous walking appears necessary for the crickets to realize the defect of their sensory system and to compensate the related escape behavior. A hypothesis for the compensation mechanism based on the efference copy signal is proposed.

Organization of Receptive Fields of Cricket Giant Interneurons Revealed by Cercal Ablations

Abstract In order to determine the contribution of each cercus and its receptors in organizing the receptive field of four air-motion sensitive giant interneurons (GIs 8–1, 9–1, 9–2 and 9–3) of the cricket Gryllus bimaculatus, effects of removing the ipsilateral or contralateral cercus (referred to the side of the axons) on specific parameters of the wind-evoked responses of these neurons were investigated. All 4 GIs received only excitatory inputs from a group of filiform hairs on the ipsilateral cercus. In addition to the ipsilateral excitatory inputs, GIs 8–1 and 9–1 received weak excitatory and strong inhibitory inputs from a group of filiform hairs on the contralateral cercus. GI 9–2 received only inhibitory inputs from filiform hairs on the contralateral cercus. GI 9–3 received excitatory inputs from filiform hairs on the contralateral cercus and no inhibitory input was confirmed. In addition to such simple excitatory and inhibitory connections, the rebound motion of cercal filiform hairs had some role in organizing the receptive fields of GIs 9–2 and 9–3. Furthermore, the possibility of using a rebound depolarization of the membrane potential for mediating the long latency response in GIs 8–1 and 9–2 will be discussed.

Changes in the Escape Eliciting System of a Cricket Revealed by Sensory Deprivation during Postembryonic Development

Abstract In the air-puff-evoked escape behavior of the cricket Gryllus bimaculatus, the effect of a uni-lateral cercal ablation and the process of behavioral recovery were investigated during postembryonic development. The response rate (relative occurrence of the escape behavior in response to an air puff stimulus) and the escape direction (relative to the stimulus direction) in first-, third-, sixth- and last-instar nymphs were almost identical with those of adults. A unilateral cercal ablation in the nymphs caused a decrease in the response rate and an increase in the number of misoriented escapes as have been observed in adults. However, the effect of ablation on the response rate was less in younger insects, i.e., the escape-eliciting potential of one cercus decreased during postembryonic development. Instead, facilitation of sensory inputs from both cerci essentially occurs, thus explaining the constant response rate throughout the developmental period. The response rate of the ablated insects measured after the final molt showed a compensational increase even when the cercal regenerates were removed at each molt. Although the final response rate was higher in crickets ablated from earlier stages, the recovery ratio was larger in crickets ablated from later stages. Regarding escape direction, a compensational change was observed in insects ablated from the first and the third instars. However, crickets ablated from the sixth and the last instar did not show any recovery in escape direction. The time course of the recovery in escape direction appears different between adults and nymphs.

Threshold and directional sensitivity of air-current-sensitive giant interneurons of a cricket

Some of the directional characteristics of air-current-sensitive giant interneurons (GIs) of a cricket were investigated by using an exactly defined unidirectional air-current stimulus. In each GI, the velocity thresholds for the stimulating air-current in two different directions were measured, using various time-courses of the velocity change (frequency). Each GI showed identical velocity threshold curves, depending on the stimulus direction.

Functional Recovery of Cricket Giant Interneurons after Cercal Ablations

Abstract In order to explore the functional recovery of the cercal sensory system of the cricket Gryllus bimaculatus, changes in response properties of four air-motion sensitive giant interneurons (GIs 8–1, 9–1, 9–2 and 9–3) were investigated after partial sensory deprivations. Velocity thresholds, response magnitudes and response latencies of each GI to a directional air current stimulus were investigated 21 days after ipsilateral or contralateral cercal ablations. The results were compared to those measured 1 day after the same treatment (Matsuura and Kanou, 1998) in order to specify the changes which occurred during the first 20 days. Each GI showed a different pattern of change in responses according to the direction of stimulus air current; i.e. the changes observed were direction dependent regardless of whether they were compensational or not. Compensational changes in response magnitudes and/or response latencies were observed in GIs 8–1, 9–1 and 9–2 when air currents were applied from particular directions. As there was no regeneration of cercal filiform hairs, those changes must be caused by the changes in synaptic strength between GIs and particular sensory afferents associated with cercal filiform hairs. Such neural compensation must underlie the basis of behavioral compensation when the insects have damaged sensory apparatus.

Mechanical polarization in the air-current sensory hair of a cricket

We examined the mechanical anisotropy of the basement spring which underlies the directional sensitivity of the cercal filiform hair of the cricket (Gryllus bimaculatus). Spring stiffness varied with the direction of hair deflection. The anisotropic ratios were 8 for short hairs and 4 for long ones, whereas the absolute values of spring stiffness varied 100-fold with hair length.

Effects of Self-Generated Wind on Compensational Recovery of Escape Direction in Unilaterally Cercus-Ablated Crickets, Gryllus bimaculatus

Abstract The effects of self-generated wind on the compensational recovery of escape direction were investigated in unilaterally cercus-ablated crickets, Gryllus bimaculatus. To separate walking and self-generated wind during walking, unilaterally cercus-ablated crickets were placed on a styrofoam ball that was easily rotated by leg motion during walking. The stationary walking on the ball did not produce self-generated wind, because no body motion occurred. Crickets that were trained on the ball but given no artificial air puff for 14 days after cercal ablation did not show any compensational recovery of escape direction. Therefore, spontaneous walking itself was not sufficient to compensate the wind-evoked escape direction in the crickets. Artificial air puffs from the anterior direction synchronized with the stationary walking were effective for the compensational recovery of escape direction, but those from the posterior direction were not. As most of the spontaneous walking was directed to the forward direction, only an artificial air puff from the anterior direction coincided well with actual self-generated wind occurring during the onset of normal walking. Therefore, self-generated wind during walking seems essential for the compensational recovery of escape direction in unilaterally cercus-ablated crickets. When artificial air puffs were unsynchronized with walking, no compensational recovery was observed. This result suggests that artificial air puffs should be given just after the onset of spontaneous walking. Otherwise, the artificial air puffs may not be recognized as self-generated wind.