Anatol G. Feldman. Referent control of action and perception. Challenging conventional theories in behavioral neuroscience

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2 Anatol G. Feldman Referent control of action and perception Challenging conventional theories in behavioral neuroscience

3 Referent control of action and perception

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5 Anatol G. Feldman Referent control of action and perception Challenging conventional theories in behavioral neuroscience

6 Anatol G. Feldman Department of Neuroscience University of Montreal Center for Interdisciplinary Reseach in Rehabilitation Montreal, QC, Canada ISBN DOI / ISBN (ebook) Library of Congress Control Number: Springer New York Heidelberg Dordrecht London Springer Science+Business Media New York 2015 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. Printed on acid-free paper Springer Science+Business Media LLC New York is part of Springer Science+Business Media (

7 Contents Preamble: The Meaning of the Term Referent Control... xiii 1 Running Away from KGB Informers to Neuroscience Switching from Physics to Neuroscience Moscow Biological School Action and Perception in the Context of Physical Laws The Purpose of Scientific Inquiry About Action and Perception Harmonizing Motor Actions with Physical Laws Law-Constrained Variables and Parameters of Physical Laws Harmonizing Control of Actions with Physical Laws Parametric Control of Posture and Movement Remarkable Features of Parametric Control Questioning the Validity of the Efference Copy Concept for Motor Control A Historically Perpetuated Error in Thinking About How Motor Actions Are Controlled Perception in the Context of Physical Laws Referent Control as a Specific Form of Parametric Control of Actions: Empirical Demonstrations Earlier Demonstrations of Referent Control in Humans Referent Control of Actions in Animals Control of Spatial Thresholds of Reflexes: Matthews (1959) Experiments Descending Brain Systems Control Spatial Thresholds for Muscle Activation Neither Central, nor Afferent Influences Per Se Pre- determine Motor Commands to Muscles v

8 vi Contents Is Referent Control Compatible with Results of Deafferentation? Referent Control Underlies Both Slow and Fast Movements Threshold Position Resetting: A Fundamental Control Principle Underlying Both Slow and Fast Movements Changes in the Referent Arm Configuration Underlie Arm Reaching Movement Shifts in the Referent Position of Body Segments Result in Motor Action Referent Control of Actions by the Corticospinal System in Humans Intentional Changes in the Wrist Joint Angle Corticospinal Influences During the Unloading Reflex The Motoneuronal Pool in the Context of Referent Control Spatial Recruitment of Motoneurons The Range of Threshold Position Control Muscle Activation in Dynamics Neurological Motor Disorders Resulting from Deficits of Referent Control Referent Control of Agonist and Antagonist Muscles Other Dynamic Aspects of Referent Control What Comes First: Muscle Activation or Shifts in the Equilibrium Point? Gradual Shift in the Equilibrium State: Importance for Regulation of Movement Extent, Speed, Duration and Rapid Action Sequences Threshold Control as an Optimal Control of Actions Major Departures from Conventional Views on Motor Control Descending Systems Influence but Do Not Pre- determine Motor Commands or Kinematics The First Clue to How the Nervous System Solves Redundancy Problems Physiological Origin and Feed-Forward Nature of Referent Control Physiological Origin of Referent (Threshold Position) Control Taking Advantage of the Feed-Forward Nature of Referent Control During Motor Learning Feed-Forward Setting of Thresholds in Anticipation of Perturbation (TMS Studies) Further Implications of the Feed-Forward Nature of Referent Control Different Forms of Referent Control The Physiological Origin of Different Forms of Referent Control... 98

9 Contents vii The Basic Neurophysiological Rule The Referent Body Configuration Referent Coactivation Command The Referent Body Location in the Environment The Referent Body Orientation Relative to Gravity Direction Other Forms of Referent Control Referent Control of Motionless Actions Grip Force Production Pushing Against a Wall Referent Control of Movement Vertical Jumps Sit-to-Stand Movements Arm Reaching Movements Referent, Equilibrium and Actual Hand Trajectories Adaptation of Reaching Movements to Gravity: A Possible Role of Proprioception Referent Corrections of Reaching Movements: Feed-Forward Aspects Referents as Attributes of Physical Frames of Reference Physical Versus Mathematical Frames of Reference Transitions from One to Another Frame of Reference Optimality of Actions in the Context of Referent Control Synergies in the Context of Referent Control Testing the Principle of Biomechanical Correspondence Solutions to Classical Problems in the Control of Motor Actions Mechanical Reductionism in Behavioral Neuroscience The Posture-Movement Problem Converting Posture-Stabilizing to Movement-Producing Mechanisms Referent Control of Muscle Co-activation in the Context of the Posture-Movement Relationship Hybrid Schemes of Action Control: Are They Physiologically Feasible? Specifying a Particular Position or Isometric Torque Central Pattern Generators in the Context of Referent Control A Major Problem of the Existing CPG Concept Integration of Central and Afferent Signals in Normal Conditions Re-defining the CPG Concept Resetting of Spatial Thresholds Versus Gating of Reflexes

10 viii Contents Control of Posture and Gait May Not Rely on Internal Representations of the Center of Body Mass or Base of Support Sherrington s Versus Graham Brown s Views on Sensorimotor Integration: A Contest Without a Winner The Relationship Between Postural and Gait Stability Human Gait Remains Stable at Every Instance Posture and Movement Are Stabilized by Common Mechanisms Referent Control in the Context of the Dynamic Systems Theory Testing Some Aspects of Referent Control of Human Gait Permanent Phase Resetting of Gait Rhythm in Response to Perturbation Minimization of Activity of Leg Muscles at Specific Phases of Gait Referent Control of Body Shape and Swimming in Lampreys More About Stability of Posture and Movement Referent Control Ensures Stability of Posture and Movement Despite Electromechanical and Reflex Delays Typical Errors in Evaluations of Stiffness and Damping Movement Equifinality and Its Violations in the Context of Referent Control Effects of Coriolis Force as Evidence That No Internal Models of Force Fields Are Built During Motor Learning Redundancy Problems Fundamental Role of the Environment in Solving Redundancy Problems Multi-muscle Control Without Redundancy Problems Control of Reaching Movements Without Redundancy Problems Possible Neural Basis of Referent Control of Reaching The Minimization Principle and Rank-Ordered Timing of Different Forms of Referent Control Involved in Reaching Other Approaches to Redundancy Problems From Intention to Action: The Mapping Problem, Its Solution and Relation to Redundancy Problems Visio-Control Mapping for Locomotion Learning, Memory and Physical Properties of the Environment in Referent Control Action-Perception Coupling Position Sense and Sense of Effort

11 Contents ix Position Sense Rule Position Sense in Different Conditions Kinesthetic Illusions Elicited by Tendon Vibration Phantom Limb Phenomenon and Mirror Therapy of Phantom Limb Pain Kinesthetic Illusions Resulting from Electrical Brain Stimulation (Phantom Person and Awareness of Motion) Position Sense and Sense of Effort Predictive Nature of the Position Sense Rule The Referent Body Configuration as a Basis for the Body Schema Reaching Different Body Sites in Humans and Spinal Frogs Information Transmitted by Ascending Pathways to the Brain Referent Control of Eye Movements Referent Control of Gaze Controversies About the Existence of Stretch Reflexes in External Ocular Muscles Referent Control of Pursuit and Saccadic Eye Movements Questioning the Feasibility of the Pulse-Step Model for Motor Control Visual Constancy Referent Control of Optomotor Behaviors in Insects Referent Control of Body Turns The Optomotor Reflex Self-Initiated Body Turns Visual Constancy Afterword: Major Lessons and Perspectives References Index

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13 About the Author Dr. Anatol G. Feldman is one of the world s foremost neuroscientists in the area of motor control. His work has had a strong and sustained influence in behavioral neuroscience since the 1960s when he published a unique theory of motor control called the equilibrium-point hypothesis. He has been a professor in the Department of Physiology (now Neuroscience) at the University of Montreal since After having been denied the right to travel out of the USSR for 25 years, he was granted permission to attend a neuroscience meeting as a distinguished Keynote Speaker in Ontario in He returned to Canada as a visiting professor at McGill University in In 1997, he joined the Centre de recherche en sciences neurologiques (CRSN) in the Department of Neuroscience at the Université de Montréal. His laboratories are affiliated with the Center for Interdisciplinary Research in Rehabilitation of Greater Montreal (CRIR). He is the first recipient of the Nicolai Bernstein award from the International Society of Motor Control. xi

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15 Preamble: The Meaning of t he Term Referent Control Since Descartes ( ; see Descartes 2001), movements of material objects have been described in appropriate coordinate systems or frames of reference (FRs). The major idea of this book is that FRs used by the nervous system are not mathematical abstractions but physiological structures comprised of neurons that receive FR-specific sensory information. As confirmed by rigorous experimental testing, each physiological FR has attributes (parameters) that characterize its geometry, referent or origin point, and metrics that define the order of recruitment of neurons in this FR. By changing the attributes of spatial FRs, particularly their origin (referent) points, neural control levels predetermine the spatial boundaries within which action and perception can emerge, while reserving the possibility of referent corrections if the evolving action and perception do not meet the task demand. This is the essence of the notion of referent control. All motoneurons (MNs) of a single muscle are constrained to work in a spatial FR in which their rank-ordered recruitment begins at a specific, threshold muscle length. The threshold length represents the origin of this spatial FR. Spinal and supraspinal levels set or reset this origin in a task-specific way. Another physiological FR is comprised of neurons that, taken together, are able to influence the configuration of the body in physiologically possible ways. Neural control levels are able to set a particular configuration called the referent body configuration. It plays the role of the origin of this FR such that the activity of each muscle is generated or not depending on the deviation of the actual body configuration from its referent configuration. This deviation represents a global factor that allows the nervous system to control all muscles of the body as a coherent unit, without deciding which muscles should participate and how they should be activated to execute a motor action. This is an important feature of referent control, an alternative to the traditional belief that neural control levels directly preprogram biomechanical characteristics, including which muscle should be involved and how they should be activated in motor actions. The referent control in general and the choice of a referent body configuration in particular are produced by changing the intrinsic, sub-threshold state of neurons, xiii