Proprioceptive feedback reinforces centrally generated stepping patterns in the cockroach

Abstract

SUMMARYThe relative importance of sensory input for the production of centrally generated motor patterns is crucial to our understanding of how animals coordinate their body segments to locomote. In legged locomotion, where terrain heterogeneity may require stride-by-stride changes in leg placement, evidence suggests that sensory information is essential for the timing of leg movement. In a previous study we showed that in cockroaches, renowned for rapid and stable running, a coordinated pattern can be elicited from the motor centres driving the different legs in the absence of sensory feedback. In the present paper, we assess the role of movement-related sensory inputs in modifying this central pattern. We studied the effect of spontaneous steps as well as imposed transient and periodic movements of a single intact leg, and demonstrate that, depending on the movement properties, the resulting proprioceptive feedback can significantly modify phase relationships among segmental oscillators of other legs. Our analysis suggests that feedback from front legs is weaker but more phasically precise than from hind legs, selectively transferring movement-related information in a manner that strengthens the inherent rhythmic pattern and modulates local perturbations.

Recovery of locomotion after injury inDrosophiladepends on proprioception

“…In addition, this observation posits a fine-grained behavioral manifestation of proprioceptive defects. A number of studies have shown that deciphering forces and proprioceptive feedback are important in generating stable patterns or gaits (Pearson, 1972;Ridgel et al, 2000;Zill et al, 2004;Fuchs et al, 2012) (for a review from a modeling perspective, see Holmes et al, 2006; for a review with a more biological perspective, see Delcomyn, 2004) and may 'directly influence [central pattern generators] and motoneurons to maintain phase relations in a decentralized, peripheral manner' (Holmes et al, 2006) through feedback. Proprioception has also been implicated in walking direction, for example, in stick insects (Akay et al, 2007).…”

The comparative investigation of the stick insect and cockroach models in the study of insect locomotion

“…Such signals not only contribute to coordination of the joints actuating each leg, but also help establish inter-leg coordination, as demonstrated by providing controlled sensory inputs to reduced, deafferented preparations during pharmacologically induced fictive walking-like motor patterns (e.g. [35]), or by manipulating specific sensory inputs in intact, walking preparations (e.g. [33,36 ]).…”

“…Such reductions combine or blur biophysical details, but their efficacy can be tested. Specifically, phase-responsecurves, which quantify the receptivity of oscillators to inputs [16,35,51 ] and are used in computing coupling functions [30,55], can be estimated experimentally. Thus, phase reduced models can be compared directly with data.…”

Fin ray sensation participates in the generation of normal fin movement in the hovering behavior of the bluegill sunfish (Lepomis macrochirus).

“…Katz and Harris-Warrick, 1990), reinforcing rhythmicity (e.g. Fuchs et al, 2012) and, as discussed above for locusts, contributing to coordination of limb elements (e.g. Grillner and Zangger, 1979) or axial segments (Wen et al, 2012).…”