Table Of ContentResearch Topics in Physiology
Charles D. Barnes, Editor
Department of Physiology
Texas Tech University School of Medicine
Lubbock, Texas
1. Donald G. Davies and Charles D. Barnes (Editors). Regulation
of Ventilation and Gas Exchange, 1978
2. Maysie J. Hughes and Charles D. Barnes (Editors). Neural Con-
trol of Circulation, 1980
3. John Orem and Charles D. Barnes (Editors). Physiology in Sleep,
1981
4. M. F. Crass, III and C. D. Barnes (Editors). Vascular Smooth
Muscle: Metabolic, Ionic, and Contractile Mechanisms, 1982
5. James J. McGrath and Charles D. Barnes (Editors). Air Pollu-
tion—Physiological Effects, 1982
6. Charles D. Barnes (Editor). Brainstem Control of Spinal Cord
Function, 1984
Brainstem Control
of Spinal Cord Function
Edited by
CHARLES D. BARNES
Department of Physiology
Texas Tech University Health Sciences Center
School of Medicine
Lubbock, Texas
1984
ACADEMIC PRESS, INC.
(Har court Brace Jovanovich, Publishers)
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COPYRIGHT © 1984, BY ACADEMIC PRESS, INC.
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ACADEMIC PRESS, INC.
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United Kingdom Edition published by
ACADEMIC PRESS, INC. (LONDON) LTD.
24/28 Oval Road, London NW1 7DX
Library of Congress Cataloging in Publication Data
Main entry under title:
Brainstem control of spinal cord function.
(Research topics in physiology)
Includes bibliographical references and index.
1. Brainstem—Addresses, essays, lectures.
2. Spinal cord—Addresses, essays, lectures. 3. Reticu-
lar formation—Addresses, essays, lectures. 4. Reflexes
—Addresses, essays, lectures. I. Barnes, Charles Dee.
II. Series. [DNLM: 1. Brainstem—Physiology.
2. Spinal cord—Physiology. Wl RE235E v. 7 / WL 310
B814]
QP376.8.B7 1983 6121.83 83-11800
ISBN 0-12-079040-8
PRINTED IN THE UNITED STATES OF AMERICA
84 85 86 87 9 8 7 6 5 4 3 2 1
Contributors
Numbers in parentheses indicate the pages on which the authors' contribu-
tions begin.
Gyan C. Agarwal (1), Department of Bioengineering, University
of Illinois at Chicago, Chicago, Illinois 60680
Charles D. Barnes* (215), Department of Physiology, Texas Tech
University Health Sciences Center, School of Medicine, Lub-
bock, Texas 79430
Simon J. Fung (215), Department of Physiology, Texas Tech Uni-
versity Health Sciences Center, School of Medicine, Lubbock,
Texas 79430
Gerald L. Gottlieb (1), Department of Physiology, Rush Medical
College, Chicago, Illinois 60612
Barry W. Peterson (27), Departments of Physiology and Rehabil-
itation Medicine, Northwestern University Medical School,
Chicago, Illinois 60611
Ottavio Pompeiano (87), Istituto di Fisiologia Umana, Université
di Pisa, 1-56100 Pisa, Italy
Susan R. White (257), Faculty of Medicine, Memorial University
of Newfoundland, St. John's, Newfoundland A1B 3V6,
Canada
William D. Willis, Jr. (141), Marine Biomedical Institute and De-
partments of Physiology and Biophysics and of Anatomy, Uni-
versity of Texas Medical Branch, Galveston, Texas 77550
*Present address: Department of Veterinary and Comparative Anatomy, Pharmacology,
and Physiology, Washington State University, Pullman, Washington 99164.
ix
Preface
With an ever-increasing number of neuroanatomical tracer
techniques based on anteriograde transport of amino acids (such as
horseradish peroxidase), our knowledge of the projections from
the brainstem into the spinal cord has expanded tremendously.
With the increase of anatomical data has come ever-accelerating
investigations into the functional aspects of these anatomical con-
nections. As a review focusing on the major bulbospinal control
systems, this volume was designed to place the most current work
in perspective by tracing its history.
The first chapter by Gottlieb and Agarwal is an attempt to put
into perspective recent findings indicating that human spinal re-
flexes are modulated from yet unspecified higher centers. In the
chapter that follows, Peterson examines the reticulospinal system,
its role in the control of movements, and its participation in
responses elicited from several sensory systems. In the third chap-
ter, Pompeiano compares the response characteristics of the ves-
tibulospinal and the medullary reticulospinal systems, emphasiz-
ing his own most recent studies on labyrinthine and neck input. In
the next chapter, which departs from the discussion of classic
bulbospinal systems, Willis examines all aspects (including motor
and sensory) of the raphe—spinal system. In Chapter 5, Fung and
Barnes discuss locus coeruleus control of spinal cord activity. The
final chapter by White deals with experimental allergic en-
cephalomyelitis, which has been considered an animal model of
multiple sclerosis. The chapter reviews the author's extensive in-
vestigations into the mechanisms by which the disease produces
hindlimb paralysis even though the animal maintains reflex activ-
ity and many spinal bulbospinal pathways remain intact.
xi
Xll Preface
Brainstem Control of Spinal Cord Function is designed for anyone
interested in the bulbar aspects of the control of spinal cord activ-
ity. It offers in-depth presentations of current theoretical and
experimental aspects of bulbospinal circuits and should prove
useful not only to those specializing in these areas but also to those
studying or researching other physiologic systems whose func-
tions are dependent on spinal cord activity.
Charles D. Barnes
1
Modulation of Human
Spinal Reflexes
Gerald L. Gottlieb
Department of Physiology
Rush Medical College
Chicago, Illinois
Gyan C. Agarwal
Department of Bioengineering
University of Illinois at Chicago
Chicago, Illinois
I. Introduction 2
II. Methods for Observing Human Reflex Responses 2
A. Step Loading Techniques 2
B. Sinusoidal Oscillation Techniques 3
C. Pseudorandom Perturbation Techniques 5
III. Responses at the Ankle, Wrist, and Elbow Joints 5
A. Short-Latency Responses 5
B. Medium-Latency Responses 7
C. Long-Latency Responses 7
D. Oscillation Responses 7
E. Pseudorandom Perturbation Responses 10
IV. Modulation of the Electromyographic Responses 12
A. Effects of Prior Contraction 13
B. Effects of Prior Instruction 16
C. Effects of Vibration 17
D. Effects of Ischemia IS
E. Effects of Local Anesthesia 21
V. Reflex Contributions to Motor Behavior 22
VI. Summary and Conclusions 24
References 25
1
BRAINSTEM CONTROL Copyright © 1984 by Academic Press, Inc.
OF SPINAL CORD FUNCTION All rights of reproduction in any form reserved.
ISBN 0-12-079040-8
2 Gerald L. Gottlieb and Gyan C. Agarwal
I. INTRODUCTION
Motor behavior is partitioned conventionally into two categories: re-
flex actions and voluntary actions.1 Although the tendon jerk is a clear
example of the former and turning the pages of this book an equally
clear example of the latter, the separation is, for many actions, prob-
lematic. In the two examples just cited, the motor behaviors in question
arise from different sources: in the one an external signal, a hammer tap
to the tendon, and in the other an internal signal, the desire to read the
next page.
The division is less clear, for example, in the case of voluntary actions
that are elicited by a mechanical stimulus. Both kinds of responses may
occur, and the issue becomes one of deciding what relative contributions
the two mechanisms make to the entire reaction. One would like, per-
haps, to look at the force occurring in a muscle after some stimulus and
be able to say that some fraction of that force was reflexic in origin, the
remainder was voluntary, and the total force is the sum of those two
parts. This chapter contends that such a separation is not entirely possi-
ble. Volition can generate muscular forces, as can adequate mechanical
stimuli. When the two converge, however, the result is not simply the
superposition of one independent response on another. It also contains
a component resulting from an interaction of the two motor signals at
the final common pathway, the α-motoneuron pool.
In functional terms this phenomenon can be described as the modula-
tion of descending control signals by sensory, reflex-evoking inputs to
the central nervous system (CNS). In terms of control theory it is more
convenient to talk in the converse, of descending control signals modu-
lating the excitability or gains of the segmental reflex arcs. The following
sections review some of the accumulated experimental evidence sup-
porting this view of motor system behavior. We conclude with a discus-
sion of its possible physiological significance to overall behavior.
II. METHODS FOR OBSERVING HUMAN
REFLEX RESPONSES
A. Step Loading Techniques
The use of rapidly applied torques or displacements to a joint is a
common technique that was first employed in studies of humans by
lr
The reflexes to be discussed are only those elicited by muscle stretch. They involve a
single agonist-antagonist muscle pair acting around a single joint. Similarly, the voluntary
1. Modulation of Human Spinal Reflexes 3
Hammond (1954). It has since been widely adopted to study human
responses in the thumb (Marsden et al, 1976), elbow (Hammond, 1956;
Hammond et al, 1956; Crago et al, 1976), and ankle (Melvill-Jones and
Watt, 1971; Gottlieb and Agarwal, 1979, 1980a,b; Gottlieb et al, 1981,
1983) as well as wrist flexion/extension (Lee and Tatton, 1975; Jaeger et
al, 1982a,b) and wrist rotation (Evarts and Vaughn, 1978).
One virtue of this technique is that the independent variable (either
joint torque or joint angle) is changed rapidly (as compared with the
latencies of any physiological responses that may occur) and then held
constant so that those responses can be more clearly detected and quan-
tified. This technique can evoke responses at essentially monosynaptic
latency at all the joints studied to date. Thus, the mechanisms of at least
one component of the response, the earliest, can be determined with
some confidence.
The responses evoked by such simple inputs are, unfortunately, not
simple. A prolonged sequence of electromyographic potentials can be
observed, with various elements of the sequence depending in different
ways on a number of experimental variables. For all of those elements
after the first, latency is no longer a useful parameter for distinguishing
among possible underlying mechanisms. Short-loop reflexes (i.e., seg-
mental), long-loop reflexes (suprasegmental, up to and including the
cerebral cortex), and volitional responses of various kinds can all con-
tribute to the evoked response. The problem in attributing any fraction
of the response of any particular neurophysiological substrate is ex-
tremely difficult. This problem is addressed in the sections that follow.
B. Sinusoidal Oscillation Techniques
In part, sinusoids are used as driving inputs for studying the motor
system because it seems appropriate to use periodic stimuli to study the
natural rhythmicities found in motor behavior (i.e., tremors). Sinusoids
have also been used profitably by engineers to investigate the behaviors
of complex systems, particularly linear systems, for which there is an
extensive body of mathematical techniques. Because of the nonlinear-
ities in the motor system, observations made after sinusoidal inputs can-
not be promptly extrapolated to predict responses to other forms of
inputs. Nonetheless, the observations obtained were in themselves suffi-
ciently interesting to have been studied by several investigators.
actions are restricted to those acting around one joint. These are the ankle, wrist, and
elbow in normal human subjects.
4 Gerald L. Gottlieb and Gyan C. Agarwal
Berthoz and Metrai (1970) examined the angular displacements and
flexor electromyograms (EMGs) of the human forearm during sinusoi-
dal torque perturbations of various frequencies. They noted that, al-
though their torque amplitudes were constant at all frequencies, the
angular displacements varied with frequencies in a characteristic man-
ner. The largest excursions were found between 3 and 5 Hz and dimin-
ished at lower and higher frequencies. Above 6 Hz, the excursions de-
creased consistently with increasing frequency. At all frequencies, the
stretch-evoked flexor EMG showed a phase lead that increased with
frequency.
In 1974 Joyce et al. and Joyce and Rack examined the same system but
used a flywheel mechanism (rather than sinusoidal torque) to generate
sinusoidal displacements of a given amplitude at all frequencies. Agar-
wal and Gottlieb (1977a) examined the human ankle joint with sinusoi-
dal torques.
The obvious oversimplification that the limb—muscle reflex system
can be approximated by an inertial mass J attached to a spring Κ and a
viscous damper Β allows the simple description by Eq. (1). Γ is resultant
joint torque and θ is joint angle.
T=J d2Q/dt2 + Β deIdt + KQ (1)
The compliance of a joint is defined as the ratio of angular displace-
ment to torque change. Linear systems described by Eq. (1) can be
Laplace-transformed to yield an expression for compliance C as a func-
tion of the complex frequency 5, as in Eq. (2).
C = Ι/ψ2 + Bs + Κ) (2)
Systems described by Eqs. (1) and (2) have a constant compliance at
low frequencies (l/K) and a compliance at high frequencies equal to
1/(/ω2), where ω is the radian frequency of oscillation. At intermediate
frequencies around a "resonant frequency" ω , defined by Eq. (3), a
β
peak in the compliance curve might appear. This would depend on the
"damping ratio" ξ, defined by Eq. (4).
A noticeable peak in the plot of compliance versus frequency occurs
for ξ less than approximately 0.5.
ω = VKJJ (3)
β
ξ - VB/2KJ (4)
Equations (1) and (2) provide succinct descriptions of the compliant
response of a joint to sinusoidal torques or displacements. Were the joint
linear (which is to say that the principal of superposition of inputs and
