Sensory feedback and coordinating asymmetrical landing in toads

Abstract

Coordinated landing requires anticipating the timing and magnitude of impact, which in turn requires sensory input. To better understand how cane toads, well known for coordinated landing, prioritize visual versus vestibular feedback during hopping, we recorded forelimb joint angle patterns and electromyographic data from five animals hopping under two conditions that were designed to force animals to land with one forelimb well before the other. In one condition, landing asymmetry was due to mid-air rolling, created by an unstable takeoff surface. In this condition, visual, vestibular and proprioceptive information could be used to predict asymmetric landing. In the other, animals took off normally, but landed asymmetrically because of a sloped landing surface. In this condition, sensory feedback provided conflicting information, and only visual feedback could appropriately predict the asymmetrical landing. During the roll treatment, when all sensory feedback could be used to predict an asymmetrical landing, pre-landing forelimb muscle activity and movement began earlier in the limb that landed first. However, no such asymmetries in forelimb preparation were apparent during hops onto sloped landings when only visual information could be used to predict landing asymmetry. These data suggest that toads prioritize vestibular or proprioceptive information over visual feedback to coordinate landing.

Evidence toads may modulate landing preparation without predicting impact time

“…While the close alignment between the forelimb angle and the velocity vector suggests active control, it could also be a passive consequence of hop dynamics or elastic energy storage. Either control strategy would be consistent with earlier work on cane toad landing control which appears to consist of some active ( Cox and Gillis, 2016 ) and some passive components ( Azizi et al . , 2014 ; Schnyer et al .…”

“…If arm angle were actively controlled, it would be consistent with the accumulating evidence that toads may prioritize vestibular or proprioceptive feedback over visual feedback to prepare for landing ( Gillis et al . , 2014 ; Cox and Gillis, 2016 ). Again, additional work that incorporated EMG data could shed more light on these questions.…”

Patterns of fluctuating asymmetry in the limbs of anurans

“…First, FA Hum may have limited impact on landing performance. Although differences in length would presumably lead to one limb contacting the ground prior to the other, thereby destabilizing the landing process by causing animals to rotate along the major body axis, animals might be able to modulate their kinematic behavior during landing to mitigate impacts of asymmetry (Cox & Gillis, ). Alternatively, it is possible that the differences in length associated with FA are not large enough to negatively impact landing performance.…”

The integration of sensory feedback in the modulation of anuran landing preparation

“…Further evidence suggests that, if toads do predict impact, they do not primarily rely on vision to do so. For instance, toads adjust the timing of landing preparation between contralateral forelimbs when their body rolls from level after takeoff, but not when the landing surface is tilted at an angle (Cox and Gillis, 2016), suggesting that toads prioritize vestibular over visual information during landing preparation. Further, ablating vestibular or proprioceptive feedback in jumping toads drastically alters or entirely eliminates landing preparation (Cox et al, 2018), whereas blinded toads were able to successfully coordinate landing, albeit with greater timing variability (Cox et al, 2018;Ekstrom et al, 2018).…”