Neuronal Control of Swimming Behavior: Comparison of Vertebrate and Invertebrate Model Systems

Swimming movements in the leech and lamprey are highly analogous, and lack homology. Thus, similarities in mechanisms must arise from convergent evolution rather than from common ancestry. Despite over 40 years of parallel investigations into this annelid and primitive vertebrate, a close comparison of the approaches and results of this research is lacking. The present review evaluates the neural mechanisms underlying swimming in these two animals and describes the many similarities that provide intriguing examples of convergent evolution. Specifically, we discuss swim initiation, maintenance and termination, isolated nervous system preparations, neural-circuitry, central oscillators, intersegmental coupling, phase lags, cycle periods and sensory feedback. Comparative studies between species highlight mechanisms that optimize behavior and allow us a broader understanding of nervous system function

Sensory Feedback Plays a Significant Role in Generating Walking Gait and in Gait Transition in Salamanders: A Simulation Study

Here, we investigate the role of sensory feedback in gait generation and transition by using a three-dimensional, neuro-musculo-mechanical model of a salamander with realistic physical parameters. Activation of limb and axial muscles were driven by neural output patterns obtained from a central pattern generator (CPG) which is composed of simulated spiking neurons with adaptation. The CPG consists of a body-CPG and four limb-CPGs that are interconnected via synapses both ipsilaterally and contralaterally. We use the model both with and without sensory modulation and four different combinations of ipsilateral and contralateral coupling between the limb-CPGs. We found that the proprioceptive sensory inputs are essential in obtaining a coordinated lateral sequence walking gait (walking). The sensory feedback includes the signals coming from the stretch receptor like intraspinal neurons located in the girdle regions and the limb stretch receptors residing in the hip and scapula regions of the salamander. On the other hand, walking trot gait (trotting) is more under central (CPG) influence compared to that of the peripheral or sensory feedback. We found that the gait transition from walking to trotting can be induced by increased activity of the descending drive coming from the mesencephalic locomotor region and is helped by the sensory inputs at the hip and scapula regions detecting the late stance phase. More neurophysiological experiments are required to identify the precise type of mechanoreceptors in the salamander and the neural mechanisms mediating the sensory modulation

Simulation and robotics studies of salamander locomotion: Applying neurobiological principles to the control of locomotion in robots

This article presents a project that aims at understanding the neural circuitry controlling salamander locomotion, and developing an amphibious salamander-like robot capable of replicating its bimodal locomotion, namely swimming and terrestrial walking. The controllers of the robot are central pattern generator models inspired by the salamander's locomotion control network. The goal of the project is twofold: (1) to use robots as tools for gaining a better understanding of locomotion control in vertebrates and (2) to develop new robot and control technologies for developing agile and adaptive outdoor robots. The article has four parts. We first describe the motivations behind the project. We then present neuromechanical simulation studies of locomotion control in salamanders. This is followed by a description of the current stage of the robotic developments. We conclude the article with a discussion on the usefulness of robots in neuroscience research with a special focus on locomotion contro

A kinematic and computational study of leech crawling: Support for a CPG based on travelling waves of excitation.

Many well characterized central pattern generators (CPGs) underlie behaviors (e.g., swimming, flight, heartbeat) that require regular rhythmicity and strict phase relationships. Here, we examine the organization of a CPG for leech crawling, a behavior whose success depends more on its flexibility than on its precise coordination. We examined the organization of this CPG by first characterizing the kinematics of crawling steps in normal and surgically manipulated animals, then by exploring its features in a simple neuronal model. The behavioral observations revealed the following. (1) Intersegmental coordination varied considerably with step duration, whereas the rates of elongation and contraction within individual segments were relatively constant. (2) Steps were generated in the absence of both head and tail brains, implying that midbody ganglia contain a CPG for step production. (3) Removal of sensory feedback did not affect step coordination or timing. (4) Imposed stretch greatly lengthened transitions between elongation and contraction, indicating that sensory pathways feed back onto the CPG. A simple model reproduced essential features of the observed kinematics. This model consisted of an oscillator that initiates propagating segmental waves of activity in excitatory neuronal chains, along with a parallel descending projection; together, these pathways could produce the observed intersegmental lags, coordination between phases, and step duration. We suggest that the proposed model is well suited to be modified on a step-by-step basis and that crawling may differ substantially from other described CPGs, such as that for swimming in segmented animals, where individual segments produce oscillations that are strongly phase-locked to one another

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 driv

Reproducing Five Motor Behaviors in a Salamander Robot With Virtual Muscles and a Distributed CPG Controller Regulated by Drive Signals and Proprioceptive Feedback

Diverse locomotor behaviors emerge from the interactions between the spinal central pattern generator (CPG), descending brain signals and sensory feedback. Salamander motor behaviors include swimming, struggling, forward underwater stepping, and forward and backward terrestrial stepping. Electromyographic and kinematic recordings of the trunk show that each of these five behaviors is characterized by specific patterns of muscle activation and body curvature. Electrophysiological recordings in isolated spinal cords show even more diverse patterns of activity. Using numerical modeling and robotics, we explored the mechanisms through which descending brain signals and proprioceptive feedback could take advantage of the flexibility of the spinal CPG to generate different motor patterns. Adapting a previous CPG model based on abstract oscillators, we propose a model that reproduces the features of spinal cord recordings: the diversity of motor patterns, the correlation between phase lags and cycle frequencies, and the spontaneous switches between slow and fast rhythms. The five salamander behaviors were reproduced by connecting the CPG model to a mechanical simulation of the salamander with virtual muscles and local proprioceptive feedback. The main results were validated on a robot. A distributed controller was used to obtain the fast control loops necessary for implementing the virtual muscles. The distributed control is demonstrated in an experiment where the robot splits into multiple functional parts. The five salamander behaviors were emulated by regulating the CPG with two descending drives. Reproducing the kinematics of backward stepping and struggling however required stronger muscle contractions. The passive oscillations observed in the salamander's tail during forward underwater stepping could be reproduced using a third descending drive of zero to the tail oscillators. This reduced the drag on the body in our hydrodynamic simulation. We explored the effect of local proprioceptive feedback during swimming and forward terrestrial stepping. We found that feedback could replace or reduce the need for different drives in both cases. It also reduced the variability of intersegmental phase lags toward values appropriate for locomotion. Our work suggests that different motor behaviors do not require different CPG circuits: a single circuit can produce various behaviors when modulated by descending drive and sensory feedback

ヒト二足歩行の神経制御機序 : 大脳皮質と脊髄神経回路の役割

学位の種別: 課程博士審査委員会委員 : （主査）東京大学教授 中澤 公孝, 東京大学准教授 柳原 大, 東京大学准教授 工藤 和俊, 東京大学准教授 吉岡 伸輔, 上武大学教授 関口 浩文University of Tokyo(東京大学