Asymmetric and transient properties of reciprocal activity of antagonists during the paw-shake response in the cat

Mutually inhibitory populations of neurons, half-center oscillators (HCOs), are commonly involved in the dynamics of the central pattern generators (CPGs) driving various rhythmic movements. Previously, we developed a multifunctional, multistable symmetric HCO model which produced slow locomotor-like and fast paw-shake-like activity patterns. Here, we describe asymmetric features of paw-shake responses in a symmetric HCO model and test these predictions experimentally. We considered bursting properties of the two model half-centers during transient paw-shake-like responses to short perturbations during locomotor-like activity. We found that when a current pulse was applied during the spiking phase of one half-center, let’s call it #1, the consecutive burst durations (BDs) of that half-center increased throughout the paw-shake response, while BDs of the other half-center, let’s call it #2, only changed slightly. In contrast, the consecutive interburst intervals (IBIs) of half-center #1 changed little, while IBIs of half-center #2 increased. We demonstrated that this asymmetry between the half-centers depends on the phase of the locomotor-like rhythm at which the perturbation was applied. We suggest that the fast transient response reflects functional asymmetries of slow processes that underly the locomotor-like pattern; e.g., asymmetric levels of inactivation across the two half-centers for a slowly inactivating inward current. We compared model results with those of in-vivo paw-shake responses evoked in locomoting cats and found similar asymmetries. Electromyographic (EMG) BDs of anterior hindlimb muscles with flexor-related activity increased in consecutive paw-shake cycles, while BD of posterior muscles with extensor-related activity did not change, and vice versa for IBIs of anterior flexors and posterior extensors. We conclude that EMG activity patterns during paw-shaking are consistent with the proposed mechanism producing transient paw-shake-like bursting patterns found in our multistable HCO model. We suggest that the described asymmetry of paw-shaking responses could implicate a multifunctional CPG controlling both locomotion and paw-shaking.

The neural bases of vertebrate motor behaviour through the lens of evolution

The primary driver of the evolution of the vertebrate nervous system has been the necessity to move, along with the requirement of controlling the plethora of motor behavioural repertoires seen among the vast and diverse vertebrate species. Understanding the neural basis of motor control through the perspective of evolution, mandates thorough examinations of the nervous systems of species in critical phylogenetic positions. We present here, a broad review of studies on the neural motor infrastructure of the lamprey, a basal and ancient vertebrate, which enjoys a unique phylogenetic position as being an extant representative of the earliest group of vertebrates. From the central pattern generators in the spinal cord to the microcircuits of the pallial cortex, work on the lamprey brain over the years, has provided detailed insights into the basic organization (a bauplan ) of the ancestral vertebrate brain, and narrates a compelling account of common ancestry of fundamental aspects of the neural bases for motion control, maintained through half a billion years of vertebrate evolution. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Overcoming a 'forbidden phenotype': The parrot's head supports, propels, and powers tripedal locomotion

No vertebrate, living or extinct, is known to have possessed an odd number of limbs. Despite this ″forbidden phenotype″, gaits that utilize odd numbers of limbs (e.g., tripedalism or pentapedalism) have evolved in both avian and mammalian lineages. Tripedal locomotion is commonly employed by parrots during climbing, who utilize their beaks as an additional support. However, it is unclear whether the beak functions simply as a stabilizing hook, or as a propulsive limb. Here, we present data on kinetics of tripedal climbing in six rosy –faced lovebirds (Agapornis rosiecollis). Our findings demonstrate that parrots utilize cyclical tripedal gaits when climbing and the beak and hindlimbs generate comparable propulsive and tangential substrate reaction forces and power. Propulsive and tangential forces generated by the beak are of equal or greater magnitudes to those forces generated by the forelimbs of humans and non –human primates during vertical climbing. We conclude that the feeding apparatus and neck musculature of parrots has been co–opted to function biomechanically as a third limb during vertical climbing. We hypothesize that this exaptation required substantive alterations to the neuromuscular system including enhanced force–generating capabilities of the neck musculature and modifications to limb central pattern generators.

Behavioral evidence for nested central pattern generator control of Drosophila grooming

Central pattern generators (CPGs) are neurons or neural circuits that produce periodic output without requiring patterned input. More complex behaviors can be assembled from simpler subroutines, and nested CPGs have been proposed to coordinate their repetitive elements, organizing control over different time scales. Here, we use behavioral experiments to establish that Drosophila grooming may be controlled by nested CPGs. On a short time scale (5–7 Hz, ~ 200 ms/movement), flies clean with periodic leg sweeps and rubs. More surprisingly, transitions between bouts of head sweeping and leg rubbing are also periodic on a longer time scale (0.3–0.6 Hz, ~2 s/bout). We examine grooming at a range of temperatures to show that the frequencies of both oscillations increase—a hallmark of CPG control—and also that rhythms at the two time scales increase at the same rate, indicating that the nested CPGs may be linked. This relationship holds when sensory drive is held constant using optogenetic activation, but oscillations can decouple in spontaneously grooming flies, showing that alternative control modes are possible. Loss of sensory feedback does not disrupt periodicity but slow down the longer time scale alternation. Nested CPGs simplify the generation of complex but repetitive behaviors, and identifying them in Drosophila grooming presents an opportunity to map the neural circuits that constitute them.

Adapting Highly-Dynamic Compliant Movements to Changing Environments: A Benchmark Comparison of Reflex- vs. CPG-Based Control Strategies

To control highly-dynamic compliant motions such as running or hopping, vertebrates rely on reflexes and Central Pattern Generators (CPGs) as core strategies. However, decoding how much each strategy contributes to the control and how they are adjusted under different conditions is still a major challenge. To help solve this question, the present paper provides a comprehensive comparison of reflexes, CPGs and a commonly used combination of the two applied to a biomimetic robot. It leverages recent findings indicating that in mammals both control principles act within a low-dimensional control submanifold. This substantially reduces the search space of parameters and enables the quantifiable comparison of the different control strategies. The chosen metrics are motion stability and energy efficiency, both key aspects for the evolution of the central nervous system. We find that neither for stability nor energy efficiency it is favorable to apply the state-of-the-art approach of a continuously feedback-adapted CPG. In both aspects, a pure reflex is more effective, but the pure CPG allows easy signal alteration when needed. Additionally, the hardware experiments clearly show that the shape of a control signal has a strong influence on energy efficiency, while previous research usually only focused on frequency alignment. Both findings suggest that currently used methods to combine the advantages of reflexes and CPGs can be improved. In future research, possible combinations of the control strategies should be reconsidered, specifically including the modulation of the control signal's shape. For this endeavor, the presented setup provides a valuable benchmark framework to enable the quantitative comparison of different bioinspired control principles.

Trpm5 channels encode bistability of spinal motoneurons and ensure motor control of hindlimbs in mice

Bistable motoneurons of the spinal cord exhibit warmth-activated plateau potential driven by Na+ and triggered by a brief excitation. The thermoregulating molecular mechanisms of bistability and their role in motor functions remain unknown. Here, we identify thermosensitive Na+-permeable Trpm5 channels as the main molecular players for bistability in mouse motoneurons. Pharmacological, genetic or computational inhibition of Trpm5 occlude bistable-related properties (slow afterdepolarization, windup, plateau potentials) and reduce spinal locomotor outputs while central pattern generators for locomotion operate normally. At cellular level, Trpm5 is activated by a ryanodine-mediated Ca2+ release and turned off by Ca2+ reuptake through the sarco/endoplasmic reticulum Ca2+-ATPase (SERCA) pump. Mice in which Trpm5 is genetically silenced in most lumbar motoneurons develop hindlimb paresis and show difficulties in executing high-demanding locomotor tasks. Overall, by encoding bistability in motoneurons, Trpm5 appears indispensable for producing a postural tone in hindlimbs and amplifying the locomotor output.

From Neural Command to Robotic Use: The Role of Symmetry/Asymmetry in Postural and Locomotor Activities

This article deepens a reflection on why and how symmetry/asymmetry affects the motor and postural behavior from the neural source, uterine development, child maturation, and how the notion of symmetry/asymmetry has been applied to walking robot design and control. The concepts of morphology and tensegrity are also presented to illustrate how the biological structures have been used in both sciences and arts. The development of the brain and the neuro-fascia-musculoskeletal system seems to be quite symmetric from the beginning of life through to complete maturity. The neural sources of movements (i.e., central pattern generators) are able to produce both symmetric or asymmetric responses to accommodate to environmental constraints and task requirements. Despite the fact that the human development is mainly symmetric, asymmetries already regulate neurological and physiological development. Laterality and sports training could affect natural musculoskeletal symmetry. The plasticity and flexibility of the nervous system allows the abilities to adapt and compensate for environmental constraints and musculoskeletal asymmetries in order to optimize the postural and movement control. For designing humanoid walking robots, symmetry approaches have been mainly used to reduce the complexity of the online calculation. Applications in neurological retraining and rehabilitation should also be considered.

Why Firing Rate Distributions Are Important for Understanding Spinal Central Pattern Generators

Networks in the spinal cord, which are responsible for the generation of rhythmic movements, commonly known as central pattern generators (CPGs), have remained elusive for decades. Although it is well-known that many spinal neurons are rhythmically active, little attention has been given to the distribution of firing rates across the population. Here, we argue that firing rate distributions can provide an important clue to the organization of the CPGs. The data that can be gleaned from the sparse literature indicate a firing rate distribution, which is skewed toward zero with a long tail, akin to a normal distribution on a log-scale, i.e., a “log-normal” distribution. Importantly, such a shape is difficult to unite with the widespread assumption of modules composed of recurrently connected excitatory neurons. Spinal modules with recurrent excitation has the propensity to quickly escalate their firing rate and reach the maximum, hence equalizing the spiking activity across the population. The population distribution of firing rates hence would consist of a narrow peak near the maximum. This is incompatible with experiments, that show wide distributions and a peak close to zero. A way to resolve this puzzle is to include recurrent inhibition internally in each CPG modules. Hence, we investigate the impact of recurrent inhibition in a model and find that the firing rate distributions are closer to the experimentally observed. We therefore propose that recurrent inhibition is a crucial element in motor circuits, and suggest that future models of motor circuits should include recurrent inhibition as a mandatory element.

Parameters optimization of central pattern generators for hexapod robot based on multi-objective genetic algorithm

In this article, a network of central pattern generators is used for the motion planning of a hexapod robot. There are many parameters in the planning network, which determine the motion performance of the hexapod robot. On the other hand, the network is a highly nonlinear coupling network, which is difficult to obtain optimal parameters by an analytical method. Optimizing these parameters to make the robot walk well is a multi-objective optimization process. There is a certain mutual exclusion relationship among the targets. To find a well-performing network as soon as possible, a multi-objective genetic algorithm is used for the process of parameter tuning. The hexapod robot simulation model is performed in Webots, and the motion performance parameters of the robot are obtained through built-in sensors and are also considered as mean values of the optimization algorithm. The optimization algorithm is written and run with MATLAB. Finally, the optimization algorithm and simulation results are proven by an experiment.