Leslie Theunissen

Spatial coordination of foot contacts in unrestrained climbing insects

Animals that live in a spatially complex environment such as the canopy of a tree, constantly need to find reliable foothold in three-dimensional (3D) space. In multi-legged animals, spatial co-ordination among legs is thought to improve efficiency of finding foothold by avoiding searching-movements in trailing legs. In stick insects, a ‘targeting mechanism’ has been described that guides foot-placement of hind- and middle legs according to the position of their leading ipsilateral leg. So far, this mechanism has been shown for standing and tethered walking animals on horizontal surfaces. Here, we investigate the efficiency of this mechanism in spatial limb co-ordination of unrestrained climbing animals. For this, we recorded whole-body kinematics of freely climbing stick insects and analysed foot placement in 3D space. We found that touch-down positions of adjacent legs were highly correlated in all three spatial dimensions, revealing 3D co-ordinate transfer among legs. Furthermore, targeting precision depended on the position of the leading leg. A second objective was to test the importance of sensory information transfer between legs. For this, we ablated a proprioceptive hair field signaling the levation of the leg. After ablation, the operated leg swung higher and performed unexpected searching movements. Furthermore, targeting of the ipsilateral trailing leg was less precise in anteroposterior and dorsoventral directions. Our results reveal that the targeting mechanism is used by unrestrained climbing stick insects in 3D space and that information from the trochanteral hair field is used in ipsilateral spatial co-ordination among legs.

Insects use two distinct classes of steps during unrestrained locomotion.

Background Adaptive, context-dependent control of locomotion requires modulation of centrally generated rhythmic motor patterns through peripheral control loops and postural reflexes. Thus assuming that the modulation of rhythmic motor patterns accounts for much of the behavioural variability observed in legged locomotion, investigating behavioural variability is a key to the understanding of context-dependent control mechanisms in locomotion. To date, the variability of unrestrained locomotion is poorly understood, and virtually nothing is known about the features that characterise the natural statistics of legged locomotion. In this study, we quantify the natural variability of hexapedal walking and climbing in insects, drawing from a database of several thousand steps recorded over two hours of walking time. Results We show that the range of step length used by unrestrained climbing stick insects is large, showing that step length can be changed substantially for adaptive locomotion. Step length distributions were always bimodal, irrespective of leg type and walking condition, suggesting the presence of two distinct classes of steps: short and long steps. Probability density of step length was well-described by a gamma distribution for short steps, and a logistic distribution for long steps. Major coefficients of these distributions remained largely unaffected by walking conditions. Short and long steps differed concerning their spatial occurrence on the walking substrate, their timing within the step sequence, and their prevalent swing direction. Finally, ablation of structures that serve to improve foothold increased the ratio of short to long steps, indicating a corrective function of short steps. Conclusions Statistical and functional differences suggest that short and long steps are physiologically distinct classes of leg movements that likely reflect distinct control mechanisms at work.

Comparative whole-body kinematics of closely related insect species with different body morphology

Legged locomotion through natural environments is very complex and variable. For example, leg kinematics may differ strongly between species, but even within the same species it is adaptive and context-dependent. Inter-species differences in locomotion are often difficult to interpret, because both morphological and ecological differences among species may be strong and, as a consequence, confound each others effects. In order to understand better how body morphology affects legged locomotion, we compare unrestrained whole-body kinematics of three stick insect species with different body proportions, but similar feeding ecology: Carausius morosus, Aretaon asperrimus and Medauroidea extradentata (=Cuniculina impigra). In order to co-vary locomotory context, we introduced a gradually increasing demand for climbing by varying the height of stairs in the setup. The species were similar in many aspects, for example in using distinct classes of steps, with minor differences concerning the spread of corrective short steps. Major differences were related to antenna length, segment lengths of thorax and head, and the ratio of leg length to body length. Whereas all species continuously moved their antennae, only Medauroidea executed high swing movements with its front legs to search for obstacles in the near-range environment. Although all species adjusted their body inclination, the range in which body segments moved differed considerably, with longer thorax segments tending to be moved more. Finally, leg posture, time courses of leg joint angles and intra-leg coordination differed most strongly in long-legged Medauroidea.

Motor flexibility in insects: Adaptive coordination of limbs in locomotion and near-range exploration

In recent years, research on insect motor behaviour―locomotion in particular―has provided a number of important new insights, many of which became possible because of methodological advances in motion capture of unrestrained moving insects. Behavioural analyses have not only backed-up neurophysiological analyses of the underlying mechanisms at work, they have also highlighted the complexity and variability of leg movements in naturalistic, unrestrained behaviour. Here, we argue that the variability of unrestrained motor behaviour should be considered a sign of behavioural flexibility. Assuming that variation of movement-related parameters is governed by neural mechanisms, behavioural analyses can complement neurophysiological investigations, for example by (i) dissociating distinct movement episodes based on functional and statistical grounds, (ii) quantifying when and how transitions between movement episodes occur, and (iii) dissociating temporal and spatial coordination. The present review emphasises the importance of considering the functional diversity of limb movements in insect behaviour. In particular, we highlight the fundamental difference between leg movements that generate interaction forces as opposed to those that do not. On that background, we discuss the spatially continuous modulation of swing movements and the quasi-rhythmic nature of stepping across insect orders. Based on examples of motor flexibility in stick insects, we illustrate the relevance of behaviour-based approaches for computational modelling of a rich and adaptive movement repertoire. Finally, we emphasise the intimate interplay of locomotion and near-range exploration. We propose that this interplay, through continuous integration of distributed, multimodal sensory feedback, is key to locomotor flexibility.

Learning relevant time points for time-series data in the life sciences

In the life sciences, short time series with high dimensional entries are becoming more and more popular such as spectrometric data or gene expression profiles taken over time. Data characteristics rule out classical time series analysis due to the few time points, and they prevent a simple vectorial treatment due to the high dimensionality. In this contribution, we successfully use the generative topographic mapping through time (GTM-TT) which is based on hidden Markov models enhanced with a topographic mapping to model such data. We propose an extension of GTM-TT by relevance learning which automatically adapts the model such that the most relevant input variables and time points are emphasized by means of an automatic relevance weighting scheme. We demonstrate the technique in two applications from the life sciences.

A Natural Movement Database for Management, Documentation, Visualization, Mining and Modeling of Locomotion Experiments

In recent years, experimental data on natural, un-restrained locomotion of animals has strongly increased in complexity and quantity. This is due to novel motion-capture techniques, but also to the combination of several methods such as electromyography or force measurements. Since much of these data are of great value for the development, modeling and benchmarking of technical locomotion systems, suitable data management, documentation and visualization are essential. Here, we use an example of comparative kinematics of climbing insects to propose a data format that is equally suitable for scientific analysis and sharing through web repositories. Two data models are used: a relational model (SQL) for efficient data management and mining, and the Resource Description Framework (RDF), releasing data according to the Linked Data principles and connecting it to other datasets on the web. Finally, two visualization options are presented, using either a photo-realistic rendering or a plain but versatile cylinder-based 3D-model.