The Organization and Role During Locomotion of the Proximal Musculature of the Cricket Foreleg. II. Electromyographic Activity During Stepping Patterns

A description is made of the patterns of electrical activity in the proximal muscles of the cricket foreleg during restrained locomotion and seeking movements, while the animal is held by the mesonotum, allowing the legs complete freedom of movement. 1. The initiation of the swing phase corresponds to the onset of the abductor muscle activity (Fig. 1). Its duration is matched by that of abduction-promotion and does not depend on the step frequency. Leg position is more variable at the end of the stance than at the end of the swing. 2. The promotor and abductor muscle activities are linked (Fig. 2). At least three units can be distinguished in each and the duration of their bursts is independent of the period (Fig. 3). 3. In the double depressors of the trochanter, muscles 77-lb,c (Fig. 4), one unit per muscle was identified, bursting during the swing phase. The duration of the burst is independent of the period. Some isolated potentials occasionally occur during the stance phase. 4. The overall activity in the lateral and medial remotors is coupled to the period; three main patterns can be described, depending upon the muscle bundle and the velocity of movement (Fig. 5). 5. In the coxal depressors two patterns of activity are described which depend on velocity of stepping (Fig. 6): (i) during regular and fast stepping (at frequencies greater than 2–5 Hz), the activity is coupled to that of the double depressors; (ii) during slow or irregular stepping, the activity is biphasic: an initial burst is followed after a latency correlated to the period by a second one in the second half of the stance phase. Conversely, the latency between the end of the second burst and the onset of the following abductor burst does not depend on the period. In most cases, a fast neurone (large amplitude, short phasic activation) is recruited when a slow one reaches high rates of discharge

Central Generation of Grooming Motor Patterns and Interlimb Coordination in Locusts

Coordinated bursts of leg motoneuron activity were evoked in locusts with deefferented legs by tactile stimulation of sites that evoke grooming behavior. This suggests that insect thoracic ganglia contain central pattern generators for directed leg movements. Motoneuron recordings were made from metathoracic and mesothoracic nerves, after eliminating all leg motor innervation, as well as all input from the brain, subesophageal ganglion, and prothoracic ganglion. Strong, brief trochanteral levator motoneuron bursts occurred, together with silence of the slow and fast trochanteral depressor motoneurons and activation of the common inhibitor motoneuron. The metathoracic slow tibial extensor motoneuron was active in a pattern distinct from its activity during walking or during rhythms evoked by the muscarinic agonist pilocarpine. Preparations in which the metathoracic ganglion was isolated from all other ganglia could still produce fictive motor patterns in response to tactile stimulation of metathoracic locations. Bursts of trochanteral levator and depressor motoneurons were clearly coordinated between the left and right metathoracic hemiganglia and also between the mesothoracic and the ipsilateral metathoracic ganglia. These data provide clear evidence for centrally generated interlimb coordination in an insect

Central Generation of Grooming Motor Patterns and Interlimb Coordination in Locusts

Coordinated bursts of leg motoneuron activity were evoked in locusts with deefferented legs by tactile stimulation of sites that evoke grooming behavior. This suggests that insect thoracic ganglia contain central pattern generators for directed leg movements. Motoneuron recordings were made from metathoracic and mesothoracic nerves, after eliminating all leg motor innervation, as well as all input from the brain, subesophageal ganglion, and prothoracic ganglion. Strong, brief trochanteral levator motoneuron bursts occurred, together with silence of the slow and fast trochanteral depressor motoneurons and activation of the common inhibitor motoneuron. The metathoracic slow tibial extensor motoneuron was active in a pattern distinct from its activity during walking or during rhythms evoked by the muscarinic agonist pilocarpine. Preparations in which the metathoracic ganglion was isolated from all other ganglia could still produce fictive motor patterns in response to tactile stimulation of metathoracic locations. Bursts of trochanteral levator and depressor motoneurons were clearly coordinated between the left and right metathoracic hemiganglia and also between the mesothoracic and the ipsilateral metathoracic ganglia. These data provide clear evidence for centrally generated interlimb coordination in an insect

Locomotor Network Dynamics Governed By Feedback Control In Crayfish Posture And Walking

Sensorimotor circuits integrate biomechanical feedback with ongoing motor activity to produce behaviors that adapt to unpredictable environments. Reflexes are critical in modulating motor output by facilitating rapid responses. During posture, resistance reflexes generate negative feedback that opposes perturbations to stabilize a body. During walking, assistance reflexes produce positive feedback that facilitates fast transitions between swing and stance of each step cycle. Until recently, sensorimotor networks have been studied using biomechanical feedback based on external perturbations in the presence or absence of intrinsic motor activity. Experiments in which biomechanical feedback driven by intrinsic motor activity is studied in the absence of perturbation have been limited. Thus, it is unclear whether feedback plays a role in facilitating transitions between behavioral states or mediating different features of network activity independent of perturbation. These properties are important to understand because they can elucidate how a circuit coordinates with other neural networks or contributes to adaptable motor output. Computational simulations and mathematical models have been used extensively to characterize interactions of negative and positive feedback with nonlinear oscillators. For example, neuronal action potentials are generated by positive and negative feedback of ionic currents via a membrane potential. While simulations enable manipulation of system parameters that are inaccessible through biological experiments, mathematical models ascertain mechanisms that help to generate biological hypotheses and can be translated across different systems. Here, a three-tiered approach was employed to determine the role of sensory feedback in a crayfish locomotor circuit involved in posture and walking. In vitro experiments using a brain-machine interface illustrated that unperturbed motor output of the circuit was changed by closing the sensory feedback loop. Then, neuromechanical simulations of the in vitro experiments reproduced a similar range of network activity and showed that the balance of sensory feedback determined how the network behaved. Finally, a reduced mathematical model was designed to generate waveforms that emulated simulation results and demonstrated how sensory feedback can control the output of a sensorimotor circuit. Together, these results showed how the strengths of different approaches can complement each other to facilitate an understanding of the mechanisms that mediate sensorimotor integration

Detection of Forces and Body Load in Standing and Walking in the American Cockroach

Sense organs in the legs that detect body weight are an important component in the regulation of posture and locomotion. This thesis seeks to gain an understanding of how body weight is detected by sense organs of the legs, and determine how this information influences muscle activities in standing and walking. The first study tested the ability of tibial campaniform sensilla (receptors that monitor forces in the cockroach leg) to encode variations in body load using magnets attached to the thorax. Recordings of sensory activities in freely standing animals showed that proximal tibial sensilla (oriented perpendicular to the leg long axis) encode the level of body load while distal receptors (oriented parallel) fired to decreasing loads. In some postures, sensillum discharges paralleled changes in activity of the trochanteral extensor muscle consistent with a known interjoint reflex. These findings demonstrate that tibial campaniform sensilla can monitor the effects of body weight upon the legs and may aid in generating support of body load. In the second study, sensory activities were compared when animals walked freely in an arena, or upon an oiled glass plate with their body weight supported. Sensilla discharges persisted but were abbreviated when body load was reduced. The results suggest that sensory discharges early in stance result from forces generated by contractions of muscles that press the leg against the substrate. Force feedback later in stance may adjust motor output to changes in loading. In the third study, muscle activities and leg movements were recorded before and after denervation of distal leg segments. Regular bursts occurred in motoneurons to leg extensor muscles following denervation, including ‘fictive’ bursting in a muscle whose tendon (apodeme) was cut in the ablation. Similar motoneuron activities were found in walking on an oiled glass surface, when effects of body weight and mechanical coupling were minimized. When distal segments were completely severed, leg use and muscle bursting were disrupted but could be restored if the stumps were pressed against the substrate. These results support the hypothesis that feedback from receptors in proximal leg segments, that indicate forces, allow for active leg use in walking

Spinal circuits can accommodate interaction torques during multijoint limb movements

The dynamic interaction of limb segments during movements that involve multiple joints creates torques in one joint due to motion about another. Evidence shows that such interaction torques are taken into account during the planning or control of movement in humans. Two alternative hypotheses could explain the compensation of these dynamic torques. One involves the use of internal models to centrally compute predicted interaction torques and their explicit compensation through anticipatory adjustment of descending motor commands. The alternative, based on the equilibrium-point hypothesis, claims that descending signals can be simple and related to the desired movement kinematics only, while spinal feedback mechanisms are responsible for the appropriate creation and coordination of dynamic muscle forces. Partial supporting evidence exists in each case. However, until now no model has explicitly shown, in the case of the second hypothesis, whether peripheral feedback is really sufficient on its own for coordinating the motion of several joints while at the same time accommodating intersegmental interaction torques. Here we propose a minimal computational model to examine this question. Using a biomechanics simulation of a two-joint arm controlled by spinal neural circuitry, we show for the first time that it is indeed possible for the neuromusculoskeletal system to transform simple descending control signals into muscle activation patterns that accommodate interaction forces depending on their direction and magnitude. This is achieved without the aid of any central predictive signal. Even though the model makes various simplifications and abstractions compared to the complexities involved in the control of human arm movements, the finding lends plausibility to the hypothesis that some multijoint movements can in principle be controlled even in the absence of internal models of intersegmental dynamics or learned compensatory motor signals.This work is funded by the project "eSMCs: Extending Sensorimotor Contingencies to Cognition," FP7-ICT-2009-6 no: 270212

A study of autonomy in decapod crustacea

Autotomy is the process whereby an animal can discard a part of it's body from a preformed breakage plane. This study examines the natural occurrence of limb autotomy in the crab Carcinus maenas in the Yealm estuary, Devon; and the nervous control of limb autotomy in the hermit crab Pagurus bernhardus and the shore crab Carcinus maenas. Of the crabs caught in the Yealm estuary in monthly samples between February 1976 and January 1977, 13.2% had lost one or more limbs, with males showing a greater incidence of autotomy (14.5%) than females (12.2%). There is a significant positive relationship between crab's size and incidence of autotomy and seasonal changes in the incidence of autotomy can be explained in terms of alterations of the mean size of crabs caught in each monthly sample. Limb autotomy in Pagurus and Carcinus results from limb injury and coactivation of the two BI levator muscles. The smaller posterior levator muscle (PL) rotates to direct isometric force from the large anterior levator muscle (AL) onto a plug in the breakage plane which encircles the BI and cause autotomy. During normal locomotion, although the PL muscle is electrically active it's tendon does not rotate and AL force is directed away from the plug in the breakage plane. The nervous control of limb autotomy is a combination of injury induced central command and feedback from a peripheral sense organ. Injury causes high frequency excitation of AL motor neurones and inhibition of PL motor neurones. The PL muscle rotates, as during autotomy, when the sense organ CSD1 is stimulated by strong isometric contractions of the AL muscle. This investigation shows that PL rotation at autotomy results from such stimulation of CSD1 and not central nervous command. Accidental autotomy in inappropriate circumstances is prevented when CSD 1 inhibits AL contraction, inhibition which is avoided by injury induced excitation of AL motor neurones to cause autotomy.<p

Integrative Biomimetics of Autonomous Hexapedal Locomotion

Dürr V, Arena PP, Cruse H, et al. Integrative Biomimetics of Autonomous Hexapedal Locomotion. Frontiers in Neurorobotics. 2019;13: 88.Despite substantial advances in many different fields of neurorobotics in general, and biomimetic robots in particular, a key challenge is the integration of concepts: to collate and combine research on disparate and conceptually disjunct research areas in the neurosciences and engineering sciences. We claim that the development of suitable robotic integration platforms is of particular relevance to make such integration of concepts work in practice. Here, we provide an example for a hexapod robotic integration platform for autonomous locomotion. In a sequence of six focus sections dealing with aspects of intelligent, embodied motor control in insects and multipedal robots—ranging from compliant actuation, distributed proprioception and control of multiple legs, the formation of internal representations to the use of an internal body model—we introduce the walking robot HECTOR as a research platform for integrative biomimetics of hexapedal locomotion. Owing to its 18 highly sensorized, compliant actuators, light-weight exoskeleton, distributed and expandable hardware architecture, and an appropriate dynamic simulation framework, HECTOR offers many opportunities to integrate research effort across biomimetics research on actuation, sensory-motor feedback, inter-leg coordination, and cognitive abilities such as motion planning and learning of its own body size

Tarsal intersegmental reflex responses in the locust hind leg

Locomotion is vital for vertebrates and invertebrates to survive. However, the mechanisms for locomotion are partially unknown. Central Pattern Generators and reflex systems have been shown to be the basis of most movements performed by arthropods. Much has been investigated lately on Central Pattern Generators, but little work has been done in reflex systems. Locomotion and motor output in feet (or tarsus in arthropods) has also been disregarded in research. Despite that feet are responsible for stability and agility in most animals, research on feet movements is scarce.In this thesis the tarsal intersegmental reflex of the locust hind leg is investigated. The tarsal reflex consists of a response in the tarsus when there is a change in the femoro-tibial joint. The main objective of the thesis is to describe the system and to develop mathematical and experimental methods to study, model and analyse it. Through a set of experiments is shown that as the knee joint is extended, the tarsus is depressed, and as the knee joint flexes, the tarsus levates. The experiments demonstrated that there is a purely neuronal link between the femoro-tibial joint position and the tibio-tarsal joint position. Moreover, it also reveals the effect of neuromodulatory compounds, such as dopamine, serotonin or octopamine. The tarsal reflex responses are fairly consistent across individuals, although significant variability across animals was found.To model a system where variability is an issue, a mathematical model with strong generalisation abilities is used: Artificial Neural Networks (ANNs). To design the ANNs, a metaheuristic algorithm has been implemented. The resulting ANNs are shown to be as accurate as other mathematical models used in physiology when used in a well known reflex system, the FETi responses. This results showed that ANNs are as good as Wiener methods in predicting responses and they outperform them in prediction of Gaussian inputs. Furthermore, they are able to predict responses in different animals, independently of the variability, with a more limited performance.New experimental methods are also designed to obtain accurate recordings of tarsal movements in response to knee joint changes. These experimental methods facilitate the data acquisition and its accuracy, reducing measurement errors. Using the mathematical methods validated, these responses are modelled and studied, showing responses to Gaussian and sinusoidal inputs, variability across individuals and effects of neuromodulators.With the tarsal reflex described and modelled, it can be used as a tool for further research in disciplines such as medicine, in the diagnose and treatment of euromuscular dysfunction or design of prosthesis and orthoses. This model can also be implemented in robotics to aid in stability when walking on irregular terrain

Decentralised Compliant Control for Hexapod Robots: A Stick Insect Based Walking Model

Institute of Perception, Action and BehaviourThis thesis aims to transfer knowledge from insect biology into a hexapod walking robot. The similarity of the robot model to the biological target allows the testing of hypotheses regarding control and behavioural strategies in the insect. Therefore, this thesis supports biorobotic research by demonstrating that robotic implementations are improved by using biological strategies and these models can be used to understand biological systems. Specifically, this thesis addresses two central problems in hexapod walking control: the single leg control mechanism and its control variables; and the different roles of the front, middle and hind legs that allow a decentralised architecture to co-ordinate complex behavioural tasks. To investigate these problems, behavioural studies on insect curve walking were combined with quantitative simulations. Behavioural experiments were designed to explore the control of turns of freely walking stick insects, Carausius morosus, toward a visual target. A program for insect tracking and kinematic analysis of observed motion was developed. The results demonstrate that the front legs are responsible for most of the body trajectory. Nonetheless, to replicate insect walking behaviour it is necessary for all legs to contribute with specific roles. Additionally, statistics on leg stepping show that middle and hind legs continuously influence each other. This cannot be explained by previous models that heavily depend on positive feedback controllers. After careful analysis, it was found that the hind legs could actively rotate the body while the middle legs move to the inside of the curve, tangentially to the body axis. The single leg controller is known to be independent from other legs but still capable of mechanical synchronisation. To explain this behaviour positive feedback controllers have been proposed. This mechanism works for the closed kinematic chain problem, but has complications when implemented in a dynamic model. Furthermore, neurophysiological data indicate that legs always respond to disturbances as a negative feedback controller. Additional experimental data presented herein indicates that legs continuously oppose forces created by other legs. This thesis proposes a model that has a velocity positive feedback control modulated via a subordination variable in cascade with a position negative feedback mechanism as the core controller. This allows legs to oppose external and internal forces without compromising inter-leg collaboration for walking. The single leg controller is implemented using a distributed artificial neural network. This network was trained with a wider range of movement to that so far found in the simulation model. The controller implemented with a plausible biologica