The neuromechanics of animal locomotion: From biology to robotics and back.

Robotics and neuroscience are sister disciplines that both aim to understand how agile, efficient, and robust locomotion can be achieved in autonomous agents. Robotics has already benefitted from neuromechanical principles discovered by investigating animals. These include the use of high-level commands to control low-level central pattern generator-like controllers, which, in turn, are informed by sensory feedback. Reciprocally, neuroscience has benefited from tools and intuitions in robotics to reveal how embodiment, physical interactions with the environment, and sensory feedback help sculpt animal behavior. We illustrate and discuss exemplar studies of this dialog between robotics and neuroscience. We also reveal how the increasing biorealism of simulations and robots is driving these two disciplines together, forging an integrative science of autonomous behavioral control with many exciting future opportunities.

NeuroMechFly, a neuromechanical model of adult Drosophila melanogaster.

Animal behavior emerges from an interaction between neural network dynamics, musculoskeletal properties and the physical environment. Accessing and understanding the interplay between these elements requires the development of integrative and morphologically realistic neuromechanical simulations. Here we present NeuroMechFly, a data-driven model of the widely studied organism, Drosophila melanogaster. NeuroMechFly combines four independent computational modules: a physics-based simulation environment, a biomechanical exoskeleton, muscle models and neural network controllers. To enable use cases, we first define the minimum degrees of freedom of the leg from real three-dimensional kinematic measurements during walking and grooming. Then, we show how, by replaying these behaviors in the simulator, one can predict otherwise unmeasured torques and contact forces. Finally, we leverage NeuroMechFly's full neuromechanical capacity to discover neural networks and muscle parameters that drive locomotor gaits optimized for speed and stability. Thus, NeuroMechFly can increase our understanding of how behaviors emerge from interactions between complex neuromechanical systems and their physical surroundings.

Combining Reflexes and External Sensory Information in a Neuromusculoskeletal Model to Control a Quadruped Robot.

This article examines the importance of integrating locomotion and cognitive information for achieving dynamic locomotion from a viewpoint combining biology and ecological psychology. We present a mammalian neuromusculoskeletal model from external sensory information processing to muscle activation, which includes: 1) a visual-attention control mechanism for controlling attention to external inputs; 2) object recognition representing the primary motor cortex; 3) a motor control model that determines motor commands traveling down the corticospinal and reticulospinal tracts; 4) a central pattern generation model representing pattern generation in the spinal cord; and 5) a muscle reflex model representing the muscle model and its reflex mechanism. The proposed model is able to generate the locomotion of a quadruped robot in flat and natural terrain. The experiment also shows the importance of a postural reflex mechanism when experiencing a sudden obstacle. We show the reflex mechanism when a sudden obstacle is separately detected from both external (retina) and internal (touching afferent) sensory information. We present the biological rationale for supporting the proposed model. Finally, we discuss future contributions, trends, and the importance of the proposed research.

AQuRo: A Cat-like Adaptive Quadruped Robot With Novel Bio-Inspired Capabilities.

There are currently many quadruped robots suited to a wide range of applications, but traversing some terrains, such as vertical ladders, remains an open challenge. There is still a need to develop adaptive robots that can walk and climb efficiently. This paper presents an adaptive quadruped robot that, by mimicking feline structure, supports several novel capabilities. We design a novel paw structure and several point-cloud-based sensory structures incorporating a quad-composite time-of-flight sensor and a dual-laser range finder. The proposed robot is equipped with physical and cognitive capabilities which include: 1) a dynamic-density topological map building with attention model, 2) affordance perception using the topological map, and 3) a neural-based locomotion model. The novel capabilities show strong integration between locomotion and internal-external sensory information, enabling short-term adaptations in response to environmental changes. The robot performed well in several situations: walking on natural terrain, walking with a leg malfunction, avoiding a sudden obstacle, climbing a vertical ladder. Further, we consider current problems and future development.

A Whole-Body Musculoskeletal Model of the Mouse.

Neural control of movement cannot be fully understood without careful consideration of interactions between the neural and biomechanical components. Recent advancements in mouse molecular genetics allow for the identification and manipulation of constituent elements underlying the neural control of movement. To complement experimental studies and investigate the mechanisms by which the neural circuitry interacts with the body and the environment, computational studies modeling motor behaviors in mice need to incorporate a model of the mouse musculoskeletal system. Here, we present the first fully articulated musculoskeletal model of the mouse. The mouse skeletal system has been developed from anatomical references and includes the sets of bones in all body compartments, including four limbs, spine, head and tail. Joints between all bones allow for simulation of full 3D mouse kinematics and kinetics. Hindlimb and forelimb musculature has been implemented using Hill-type muscle models. We analyzed the mouse whole-body model and described the moment-arms for different hindlimb and forelimb muscles, the moments applied by these muscles on the joints, and their involvement in limb movements at different limb/body configurations. The model represents a necessary step for the subsequent development of a comprehensive neuro-biomechanical model of freely behaving mice; this will close the loop between the neural control and the physical interactions between the body and the environment.

Walking with Salamanders: From Molecules to Biorobotics.

How do four-legged animals adapt their locomotion to the environment? How do central and peripheral mechanisms interact within the spinal cord to produce adaptive locomotion and how is locomotion recovered when spinal circuits are perturbed? Salamanders are the only tetrapods that regenerate voluntary locomotion after full spinal transection. Given their evolutionary position, they provide a unique opportunity to bridge discoveries made in fish and mammalian models. Genetic dissection of salamander neural circuits is becoming feasible with new methods for precise manipulation, elimination, and visualisation of cells. These approaches can be combined with classical tools in neuroscience and with modelling and a robotic environment. We propose that salamanders provide a blueprint of the function, evolution, and regeneration of tetrapod locomotor circuits.

Oncilla Robot: A Versatile Open-Source Quadruped Research Robot With Compliant Pantograph Legs.

We present Oncilla robot, a novel mobile, quadruped legged locomotion machine. This large-cat sized, 5.1 kg robot is one of a kind of a recent, bioinspired legged robot class designed with the capability of model-free locomotion control. Animal legged locomotion in rough terrain is clearly shaped by sensor feedback systems. Results with Oncilla robot show that agile and versatile locomotion is possible without sensory signals to some extend, and tracking becomes robust when feedback control is added (Ajallooeian, 2015). By incorporating mechanical and control blueprints inspired from animals, and by observing the resulting robot locomotion characteristics, we aim to understand the contribution of individual components. Legged robots have a wide mechanical and control design parameter space, and a unique potential as research tools to investigate principles of biomechanics and legged locomotion control. But the hardware and controller design can be a steep initial hurdle for academic research. To facilitate the easy start and development of legged robots, Oncilla-robot's blueprints are available through open-source. The robot's locomotion capabilities are shown in several scenarios. Specifically, its spring-loaded pantographic leg design compensates for overdetermined body and leg postures, i.e., during turning maneuvers, locomotion outdoors, or while going up and down slopes. The robot's active degree of freedom allow tight and swift direction changes, and turns on the spot. Presented hardware experiments are conducted in an open-loop manner, with little control and computational effort. For more versatile locomotion control, Oncilla-robot can sense leg joint rotations, and leg-trunk forces. Additional sensors can be included for feedback control with an open communication protocol interface. The robot's customized actuators are designed for robust actuation, and efficient locomotion. It trots with a cost of transport of 3.2 J/(Nm), at a speed of 0.63 m s-1 (Froude number 0.25). The robot trots inclined slopes up to 10°, at 0.25 m s-1. The multi-body Webots model of Oncilla robot, and Oncilla robot's extensive software architecture enables users to design and test scenarios in simulation. Controllers can directly be transferred to the real robot. Oncilla robot's blueprints are open-source published (hardware GLP v3, software LGPL v3).

Interactive locomotion: Investigation and modeling of physically-paired humans while walking.

In spite of extensive studies on human walking, less research has been conducted on human walking gait adaptation during interaction with another human. In this paper, we study a particular case of interactive locomotion where two humans carry a rigid object together. Experimental data from two persons walking together, one in front of the other, while carrying a stretcher-like object is presented, and the adaptation of their walking gaits and coordination of the foot-fall patterns are analyzed. It is observed that in more than 70% of the experiments the subjects synchronize their walking gaits; it is shown that these walking gaits can be associated to quadrupedal gaits. Moreover, in order to understand the extent by which the passive dynamics can explain this synchronization behaviour, a simple 2D model, made of two-coupled spring-loaded inverted pendulums, is developed, and a comparison between the experiments and simulations with this model is presented, showing that with this simple model we are able to reproduce some aspects of human walking behaviour when paired with another human.

Climbing favours the tripod gait over alternative faster insect gaits.

To escape danger or catch prey, running vertebrates rely on dynamic gaits with minimal ground contact. By contrast, most insects use a tripod gait that maintains at least three legs on the ground at any given time. One prevailing hypothesis for this difference in fast locomotor strategies is that tripod locomotion allows insects to rapidly navigate three-dimensional terrain. To test this, we computationally discovered fast locomotor gaits for a model based on Drosophila melanogaster. Indeed, the tripod gait emerges to the exclusion of many other possible gaits when optimizing fast upward climbing with leg adhesion. By contrast, novel two-legged bipod gaits are fastest on flat terrain without adhesion in the model and in a hexapod robot. Intriguingly, when adhesive leg structures in real Drosophila are covered, animals exhibit atypical bipod-like leg coordination. We propose that the requirement to climb vertical terrain may drive the prevalence of the tripod gait over faster alternative gaits with minimal ground contact.

Kinematic and Gait Similarities between Crawling Human Infants and Other Quadruped Mammals.

Crawling on hands and knees is an early pattern of human infant locomotion, which offers an interesting way of studying quadrupedalism in one of its simplest form. We investigate how crawling human infants compare to other quadruped mammals, especially primates. We present quantitative data on both the gait and kinematics of seven 10-month-old crawling infants. Body movements were measured with an optoelectronic system giving precise data on 3-dimensional limb movements. Crawling on hands and knees is very similar to the locomotion of non-human primates in terms of the quite protracted arm at touch-down, the coordination between the spine movements in the lateral plane and the limbs, the relatively extended limbs during locomotion and the strong correlation between stance duration and speed of locomotion. However, there are important differences compared to primates, such as the choice of a lateral-sequence walking gait, which is similar to most non-primate mammals and the relatively stiff elbows during stance as opposed to the quite compliant gaits of primates. These finding raise the question of the role of both the mechanical structure of the body and neural control on the determination of these characteristics.

Robotics and neuroscience.

In the attempt to build adaptive and intelligent machines, roboticists have looked at neuroscience for more than half a century as a source of inspiration for perception and control. More recently, neuroscientists have resorted to robots for testing hypotheses and validating models of biological nervous systems. Here, we give an overview of the work at the intersection of robotics and neuroscience and highlight the most promising approaches and areas where interactions between the two fields have generated significant new insights. We articulate the work in three sections, invertebrate, vertebrate and primate neuroscience. We argue that robots generate valuable insight into the function of nervous systems, which is intimately linked to behaviour and embodiment, and that brain-inspired algorithms and devices give robots life-like capabilities.

Kinematic primitives for walking and trotting gaits of a quadruped robot with compliant legs.

In this work we research the role of body dynamics in the complexity of kinematic patterns in a quadruped robot with compliant legs. Two gait patterns, lateral sequence walk and trot, along with leg length control patterns of different complexity were implemented in a modular, feed-forward locomotion controller. The controller was tested on a small, quadruped robot with compliant, segmented leg design, and led to self-stable and self-stabilizing robot locomotion. In-air stepping and on-ground locomotion leg kinematics were recorded, and the number and shapes of motion primitives accounting for 95% of the variance of kinematic leg data were extracted. This revealed that kinematic patterns resulting from feed-forward control had a lower complexity (in-air stepping, 2-3 primitives) than kinematic patterns from on-ground locomotion (νm4 primitives), although both experiments applied identical motor patterns. The complexity of on-ground kinematic patterns had increased, through ground contact and mechanical entrainment. The complexity of observed kinematic on-ground data matches those reported from level-ground locomotion data of legged animals. Results indicate that a very low complexity of modular, rhythmic, feed-forward motor control is sufficient for level-ground locomotion in combination with passive compliant legged hardware.

A salamander's flexible spinal network for locomotion, modeled at two levels of abstraction.

Animals have to coordinate a large number of muscles in different ways to efficiently move at various speeds and in different and complex environments. This coordination is in large part based on central pattern generators (CPGs). These neural networks are capable of producing complex rhythmic patterns when activated and modulated by relatively simple control signals. Although the generation of particular gaits by CPGs has been successfully modeled at many levels of abstraction, the principles underlying the generation and selection of a diversity of patterns of coordination in a single neural network are still not well understood. The present work specifically addresses the flexibility of the spinal locomotor networks in salamanders. We compare an abstract oscillator model and a CPG network composed of integrate-and-fire neurons, according to their ability to account for different axial patterns of coordination, and in particular the transition in gait between swimming and stepping modes. The topology of the network is inspired by models of the lamprey CPG, complemented by additions based on experimental data from isolated spinal cords of salamanders. Oscillatory centers of the limbs are included in a way that preserves the flexibility of the axial network. Similarly to the selection of forward and backward swimming in lamprey models via different excitation to the first axial segment, we can account for the modification of the axial coordination pattern between swimming and forward stepping on land in the salamander model, via different uncoupled frequencies in limb versus axial oscillators (for the same level of excitation). These results transfer partially to a more realistic model based on formal spiking neurons, and we discuss the difference between the abstract oscillator model and the model built with formal spiking neurons.

From lamprey to salamander: an exploratory modeling study on the architecture of the spinal locomotor networks in the salamander.

The evolutionary transition from water to land required new locomotor modes and corresponding adjustments of the spinal "central pattern generators" for locomotion. Salamanders resemble the first terrestrial tetrapods and represent a key animal for the study of these changes. Based on recent physiological data from salamanders, and previous work on the swimming, limbless lamprey, we present a model of the basic oscillatory network in the salamander spinal cord, the spinal segment. Model neurons are of the Hodgkin-Huxley type. Spinal hemisegments contain sparsely connected excitatory and inhibitory neuron populations, and are coupled to a contralateral hemisegment. The model yields a large range of experimental findings, especially the NMDA-induced oscillations observed in isolated axial hemisegments and segments of the salamander Pleurodeles waltlii. The model reproduces most of the effects of the blockade of AMPA synapses, glycinergic synapses, calcium-activated potassium current, persistent sodium current, and [Formula: see text]-current. Driving segments with a population of brainstem neurons yields fast oscillations in the in vivo swimming frequency range. A minimal modification to the conductances involved in burst-termination yields the slower stepping frequency range. Slow oscillators can impose their frequency on fast oscillators, as is likely the case during gait transitions from swimming to stepping. Our study shows that a lamprey-like network can potentially serve as a building block of axial and limb oscillators for swimming and stepping in salamanders.

Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics.

Vertebrate animals exhibit impressive locomotor skills. These locomotor skills are due to the complex interactions between the environment, the musculo-skeletal system and the central nervous system, in particular the spinal locomotor circuits. We are interested in decoding these interactions in the salamander, a key animal from an evolutionary point of view. It exhibits both swimming and stepping gaits and is faced with the problem of producing efficient propulsive forces using the same musculo-skeletal system in two environments with significant physical differences in density, viscosity and gravitational load. Yet its nervous system remains comparatively simple. Our approach is based on a combination of neurophysiological experiments, numerical modeling at different levels of abstraction, and robotic validation using an amphibious salamander-like robot. This article reviews the current state of our knowledge on salamander locomotion control, and presents how our approach has allowed us to obtain a first conceptual model of the salamander spinal locomotor networks. The model suggests that the salamander locomotor circuit can be seen as a lamprey-like circuit controlling axial movements of the trunk and tail, extended by specialized oscillatory centers controlling limb movements. The interplay between the two types of circuits determines the mode of locomotion under the influence of sensory feedback and descending drive, with stepping gaits at low drive, and swimming at high drive.

Dynamical movement primitives: learning attractor models for motor behaviors.

Nonlinear dynamical systems have been used in many disciplines to model complex behaviors, including biological motor control, robotics, perception, economics, traffic prediction, and neuroscience. While often the unexpected emergent behavior of nonlinear systems is the focus of investigations, it is of equal importance to create goal-directed behavior (e.g., stable locomotion from a system of coupled oscillators under perceptual guidance). Modeling goal-directed behavior with nonlinear systems is, however, rather difficult due to the parameter sensitivity of these systems, their complex phase transitions in response to subtle parameter changes, and the difficulty of analyzing and predicting their long-term behavior; intuition and time-consuming parameter tuning play a major role. This letter presents and reviews dynamical movement primitives, a line of research for modeling attractor behaviors of autonomous nonlinear dynamical systems with the help of statistical learning techniques. The essence of our approach is to start with a simple dynamical system, such as a set of linear differential equations, and transform those into a weakly nonlinear system with prescribed attractor dynamics by means of a learnable autonomous forcing term. Both point attractors and limit cycle attractors of almost arbitrary complexity can be generated. We explain the design principle of our approach and evaluate its properties in several example applications in motor control and robotics.

Where are we in understanding salamander locomotion: biological and robotic perspectives on kinematics.

Salamanders have captured the interest of biologists and roboticists for decades because of their ability to locomote in different environments and their resemblance to early representatives of tetrapods. In this article, we review biological and robotic studies on the kinematics (i.e., angular profiles of joints) of salamander locomotion aiming at three main goals: (i) to give a clear view of the kinematics, currently available, for each body part of the salamander while moving in different environments (i.e., terrestrial stepping, aquatic stepping, and swimming), (ii) to examine what is the status of our current knowledge and what remains unclear, and (iii) to discuss how much robotics and modeling have already contributed and will potentially contribute in the future to such studies.

Oscillator-based assistance of cyclical movements: model-based and model-free approaches.

In this article, we propose a new method for providing assistance during cyclical movements. This method is trajectory-free, in the sense that it provides user assistance irrespective of the performed movement, and requires no other sensing than the assisting robot's own encoders. The approach is based on adaptive oscillators, i.e., mathematical tools that are capable of learning the high level features (frequency, envelope, etc.) of a periodic input signal. Here we present two experiments that we recently conducted to validate our approach: a simple sinusoidal movement of the elbow, that we designed as a proof-of-concept, and a walking experiment. In both cases, we collected evidence illustrating that our approach indeed assisted healthy subjects during movement execution. Owing to the intrinsic periodicity of daily life movements involving the lower-limbs, we postulate that our approach holds promise for the design of innovative rehabilitation and assistance protocols for the lower-limb, requiring little to no user-specific calibration.

Human-robot synchrony: flexible assistance using adaptive oscillators.

We propose a novel method for movement assistance that is based on adaptive oscillators, i.e., mathematical tools that are capable of extracting the high-level features (amplitude, frequency, and offset) of a periodic signal. Such an oscillator acts like a filter on these features, but keeps its output in phase with respect to the input signal. Using a simple inverse model, we predicted the torque produced by human participants during rhythmic flexion-extension of the elbow. Feeding back a fraction of this estimated torque to the participant through an elbow exoskeleton, we were able to prove the assistance efficiency through a marked decrease of the biceps and triceps electromyography. Importantly, since the oscillator adapted to the movement imposed by the user, the method flexibly allowed us to change the movement pattern and was still efficient during the nonstationary epochs. This method holds promise for the development of new robot-assisted rehabilitation protocols because it does not require prespecifying a reference trajectory and does not require complex signal sensing or single-user calibration: the only signal that is measured is the position of the augmented joint. In this paper, we further demonstrate that this assistance was very intuitive for the participants who adapted almost instantaneously.