Neural Basis of Stimulus-Angle-Dependent Motor Control of Wind-Elicited Walking Behavior in the Cricket Gryllus bimaculatus

Abstract

Crickets exhibit oriented walking behavior in response to air-current stimuli. Because crickets move in the opposite direction from the stimulus source, this behavior is considered to represent ‘escape behavior’ from an approaching predator. However, details of the stimulus-angle-dependent control of locomotion during the immediate phase, and the neural basis underlying the directional motor control of this behavior remain unclear. In this study, we used a spherical-treadmill system to measure locomotory parameters including trajectory, turn angle and velocity during the immediate phase of responses to air-puff stimuli applied from various angles. Both walking direction and turn angle were correlated with stimulus angle, but their relationships followed different rules. A shorter stimulus also induced directionally-controlled walking, but reduced the yaw rotation in stimulus-angle-dependent turning. These results suggest that neural control of the turn angle requires different sensory information than that required for oriented walking. Hemi-severance of the ventral nerve cords containing descending axons from the cephalic to the prothoracic ganglion abolished stimulus-angle-dependent control, indicating that this control required descending signals from the brain. Furthermore, we selectively ablated identified ascending giant interneurons (GIs) in vivo to examine their functional roles in wind-elicited walking. Ablation of GI8-1 diminished control of the turn angle and decreased walking distance in the initial response. Meanwhile, GI9-1b ablation had no discernible effect on stimulus-angle-dependent control or walking distance, but delayed the reaction time. These results suggest that the ascending signals conveyed by GI8-1 are required for turn-angle control and maintenance of walking behavior, and that GI9-1b is responsible for rapid initiation of walking. It is possible that individual types of GIs separately supply the sensory signals required to control wind-elicited walking.

Auditory modulation of wind-elicited walking behavior in the cricket, Gryllus bimaculatus

“…1A), as described in a previous study (Oe and Ogawa, 2013). An animal was tethered on top of a Styrofoam ball using a pair of insect pins bent into an L-shape that were stuck to the cricket's tergite with paraffin wax.…”

“…Definition and calculation of these parameters were the same as those in our previous study (Oe and Ogawa, 2013). The x-and y-axes were defined as the lateral and antero-posterior axes of the cricket at the start position, respectively (Fig.…”

“…However, how spatio-temporal relationships between multiple stimuli in different modalities influence escape behaviors remains unknown. To address this question, we examined the effects of an auditory stimulus on wind-elicited walking behavior in crickets, a response that is considered to be an escape behavior (Gras and Hörner, 1992;Oe and Ogawa, 2013;Tauber and Camhi, 1995).…”

“…Oriented escape walking behavior is also elicited by the gust of air generated by an approaching predator (Gras and Hörner, 1992;Tauber and Camhi, 1995). In this behavior, the direction and turn angle of the resulting walk depends on the stimulus direction (Oe and Ogawa, 2013). However, the details of the interaction between the cercal and auditory systems are unknown.…”

Ca2+ imaging of cricket protocerebrum responses to air current stimulation

“…This implies that ascending cercal sensory information is integrated with sensory input from other modalities within a higher center that includes the protocerebrum. It was recently reported that directional control of wind-elicited walking behavior requires descending signals from the cephalic ganglia [20], and it is suggested that directional information conveyed by GIs are processed within the brain, in which some multimodal local and descending interneurons responsive to cercal stimulation have been identified [28,31]. However, the specific brain region to which GIs transmit cercal sensory information is not known, and neuronal response properties including directional selectivity have not been investigated within the brain.…”