Gaze coordination with strides during walking in the cat

Abstract

Key points Vision plays a crucial role in guiding locomotion in complex environments, but the coordination between gaze and stride is not well understood. The coordination of gaze shifts, fixations, constant gaze and slow gaze with strides in cats walking on different surfaces were examined. It was found that gaze behaviours are coordinated with strides even when walking on a flat surface in the complete darkness, occurring in a sequential order during different phases of the stride. During walking on complex surfaces, gaze behaviours are typically more tightly coordinated with strides, particularly at faster speeds, only slightly shifting in phase. These findings indicate that the coordination of gaze behaviours with strides is not vision‐driven, but is a part of the whole body locomotion synergy; the visual environment and locomotor task modulate it. The results may be relevant to developing diagnostic tools and rehabilitation approaches for patients with locomotor deficits. Abstract Vision plays a crucial role in guiding locomotion in complex environments. However, the coordination between the gaze and stride is not well understood. We investigated this coordination in cats walking on a flat surface in darkness or light, along a horizontal ladder and on a pathway with small stones. We recorded vertical and horizontal eye movements and 3‐D head movement, and calculated where gaze intersected the walkway. The coordination of gaze shifts away from the animal, gaze shifts toward, fixations, constant gaze, and slow gaze with strides was investigated. We found that even during walking on the flat surface in the darkness, all gaze behaviours were coordinated with strides. Gaze shifts and slow gaze toward started in the beginning of each forelimb's swing and ended in its second half. Fixations peaked throughout the beginning and middle of swing. Gaze shifts away began throughout the second half of swing of each forelimb and ended when both forelimbs were in stance. Constant gaze and slow gaze away occurred in the beginning of stance. However, not every behaviour occurred during every stride. Light had a small effect. The ladder and stones typically increased the coordination and caused gaze behaviours to occur 3% earlier in the cycle. At faster speeds, the coordination was often tighter and some gaze behaviours occurred 2–16% later in the cycle. The findings indicate that the coordination of gaze with strides is not vision‐driven, but is a part of the whole body locomotion synergy; the visual environment and locomotor task modulate it.

Conservation of locomotion-induced oculomotor activity through evolution in mammals

“…16 There is considerable behavioral evidence for the contribution of locomotor-related spinal signals during gaze stabilization in several mammalian species. In cats 17,18 and in humans, 19,20 locomotor signals are integrated to favor vertical eye movements by projecting gaze toward the direction of locomotion and canceling vestibulo-ocular reflex (VOR) during walking or running on a treadmill. In monkeys performing circular running in the dark, compensatory horizontal eye movements are favored by non-vestibular velocity signals.…”

Conservation of locomotion-induced oculomotor activity through evolution in higher tetrapods

“…There is considerable behavioral evidence for the contribution of locomotor-related spinal signals during gaze stabilization in several mammalian species. In cat 14,15 and in humans 16 , locomotor signals are integrated to favor vertical eye movements by projecting gaze towards the direction of locomotion and canceling VOR during walking or running on a treadmill. In monkeys performing circular running in the dark, compensatory horizontal eye movements are favored by non-vestibular velocity signals 17 .…”

When cats need to see to step accurately?

“…2017, 2018; Zubair et al . 2019). In humans, a brief denial of visual input for 400–500 ms at the end of stance increases its duration, but denial during a swing does not prolong the swing (Hollands & Marple‐Horvat, 1996), showing that acquisition, processing and use of visual information depend on the phase of the step cycle.…”

“…2014; Zubair et al . 2019). Gaze fixations occur around the middle of a forelimb swing, which is the middle of stance of the other forelimb.…”

“…Notably, qualitatively similar periodic gaze behaviour synchronized with the step cycle was observed in cats walking not only in complex environments that require vision for accurate stepping, but also on a flat surface, which does not require vision, and even when cats were walking on a flat surface in complete darkness, without any visual input (Zubair et al . 2019). Thus, control of gaze during locomotion is not just vision‐driven, but is an intrinsic component of the ongoing locomotor behaviour.…”