Behavioral context-dependent modulation of descending statocyst pathways during free walking, as revealed by optical telemetry in crayfish

Abstract

SUMMARY Crustacean posture control is based on a complex interaction between the statocyst input and other sensory inputs as well as the animal's behavioral context. We examined the effects of behavioral condition on the activity of descending statocyst pathways using an optical telemetry system that allowed underwater recording of neuronal signals from freely behaving crayfish. A functionally identified statocyst-driven interneuron that directionally responded to body tilting without a footboard and to tilting of the footboard was found to show complicated responses depending upon the ongoing behavior of the animal when it freely walked around in water on the aquarium floor. The spike firing frequency of the interneuron increased significantly during walking. When the animal stood or walked on the tilted floor, the interneuron activity represented the tilt angle and direction if the abdomen was actively flexed, but not if it was extended. Two other statocyst-driven descending interneurons were found to be affected differently by the animal's behavioral condition: the spike activity of one interneuron increased during walking, but its directional response on the tilted floor was completely absent during abdominal posture movements, whereas that of another interneuron was enhanced during abdominal extension only, representing the tilt angle and direction. The results obtained in this study provide the first experimental demonstration that crustacean postural control under natural conditions is dependent on very fine aspects of the animal's locomotor behavioral context,suggesting far more complex control mechanisms than those expected from the experimental data obtained in isolated and fixed animals.

Antagonistic Inhibitory Circuits Integrate Visual and Gravitactic Behaviors

“…In most animals, detection of gravity involves an organ with a dense mineralized mass and accompanying sensory cells. Vertebrate gravitactic organs are characterized by calcified otoliths of the vestibular system of the inner ear [4,5], although many invertebrates have mineralized statoliths that serve a similar function [6][7][8]. Gravity-sensing organs modulate a range of animal behaviors, including taxis (termed gravitaxis), posture orientation, body movements, and gaze stabilization [9][10][11].…”

Activity Patterns and Timing of Muscle Activity in the Forward Walking and Backward Walking Stick InsectCarausius morosus

“…Substantial information also exists about the central neural mechanisms that generate the locomotor output (for review, see Bässler and Büschges 1998;Büschges 2005;Büschges and Gruhn 2008), although very little is known about the timing of leg muscle activity during walking (Epstein and Graham 1983;Graham and Epstein 1985). This information is important because 1) the exact timing of muscle activities during swing-to-stance transitions is needed to assess how sensory input induces them (Büschges and Gruhn 2008) and 2) detailed knowledge of straight walking muscle activity is required to correctly interpret the alterations in muscle activity that occur during locomotor output changes such as turns (Cruse et al 2009;Gruhn et al 2009a;Mu and Ritzmann 2005;Ridgel et al 2007), changes in walking speed (Gruhn et al 2009b), and switches between tunneling and climbing (Harley et al 2009) and forward and backward walking (Akay et al 2007).…”

“…Studying neuronal or muscular activity in behaving animals requires recording techniques that do not unduly interfere with animal movement. Two techniques that have been successfully applied to relatively large animals are to use implantable electrodes and then to transmit the data along a long tether (Böhm et al 1997;Clarac et al 1987;Duch and Pflüger 1995;Gruhn and Rathmayer 2002) or using telemetric devices (Fischer et al 1996;Hama et al 2007;Kutsch et al 1993;Tsuchida et al 2004;Wang et al 2008). These methods are difficult to apply to small animals such as stick insects because smaller animals become easily entangled in the long, often heavy tethers and the weight of telemetric devices is often very large.…”

Readiness Discharge for Spontaneous Initiation of Walking in Crayfish

“…First, it can be used for activating lower modules including central pattern generators (CPGs) that generate patterned rhythmical motor outputs; it has been shown that a sustained input is required for generation of rhythmic locomotor outputs (Grillner et al, 2008). Alternatively, it can be used for sensory processing to suppress reafferent signals and/or for potentiating other behavioral acts including postural reflexes that are subsidiary to walking (Hama et al, 2007). In any case, the unit activities for initiation, continuation, and termination of walking are temporally modularized and can be used to sequentially control the self-initiated walking behavior (Fig.…”