Intersegmental coordination of cockroach locomotion: adaptive control of centrally coupled pattern generator circuits

Front Neural Circuits. 2011 Jan 20;4:125. doi: 10.3389/fncir.2010.00125. eCollection 2011.


Animals' ability to demonstrate both stereotyped and adaptive locomotor behavior is largely dependent on the interplay between centrally generated motor patterns and the sensory inputs that shape them. We utilized a combined experimental and theoretical approach to investigate the relative importance of CPG interconnections vs. intersegmental afferents in the cockroach: an animal that is renowned for rapid and stable locomotion. We simultaneously recorded coxal levator and depressor motor neurons (MN) in the thoracic ganglia of Periplaneta americana, while sensory feedback was completely blocked or allowed only from one intact stepping leg. In the absence of sensory feedback, we observed a coordination pattern with consistent phase relationship that shares similarities with a double-tripod gait, suggesting central, feedforward control. This intersegmental coordination pattern was then reinforced in the presence of sensory feedback from a single stepping leg. Specifically, we report on transient stabilization of phase differences between activity recorded in the middle and hind thoracic MN following individual front-leg steps, suggesting a role for afferent phasic information in the coordination of motor circuits at the different hemiganglia. Data were further analyzed using stochastic models of coupled oscillators and maximum likelihood techniques to estimate underlying physiological parameters, such as uncoupled endogenous frequencies of hemisegmental oscillators and coupling strengths and directions. We found that descending ipsilateral coupling is stronger than ascending coupling, while left-right coupling in both the meso- and meta-thoracic ganglia appear to be symmetrical. We discuss these results in comparison with recent findings in stick insects that share similar neural and body architectures, and argue that the two species may exemplify opposite extremes of a fast-slow locomotion continuum, mediated through different intersegment coordination strategies.

Keywords: central pattern generator; cockroach; intersegmental coordination; locomotion; maximum likelihood estimation; rostral–caudal asymmetry.