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A HISTORY OF NERVE FUNCTIONS

Recent developments have extended our knowledge of the basic functions of

nerves – notably, demonstration of the mechanism within nerve fibers that
transports a wide range of essential materials. To understand how this discov-
ery occurred, it is necessary to examine its history. The story begins in ancient
Greece when nerves were conceived of as channels through which animal
spirits carried sensory impressions to the brain. As science developed, the
discoveries of various physical and chemical agents supplanted the agency
of animal spirits until the molecular machinery of transport was recognized.
In this fascinating and complete history, Sidney Ochs begins with a chrono-
logical look at this path of discovery, followed in the second half by a the-
matic approach, wherein the author describes the electrical nature of the
nerve impulse, fiber form, and its changes in degeneration and regeneration,
reflexes, learning, memory, and other higher functions in which transport
participates. A History of Nerve Functions will serve as an invaluable resource
for historians of neuroscience and medicine, philosophers of science and
medicine, as well as for neuroscientists.

Sidney Ochs is Professor Emeritus of Cellular and Integrative Physiology at

the University of Indiana School of Medicine. He has been a pioneer in re-
search in the field of axoplasmic transport in nerves, publishing the first
monograph on the subject. He has contributed more than 300 publications
on various aspects of the peripheral and central nervous systems, including a
textbook on neurophysiology. He founded the Journal of Neurobiology and was
a Regional Organizer in the establishment of the Society for Neuroscience, as
well as later acting as a Councilor of the Society.

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A HISTORY OF NERVE FUNCTIONS

From Animal Spirits to Molecular Mechanisms

SIDNEY OCHS
Indiana University

iii
cambridge university press
Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo

Cambridge University Press

The Edinburgh Building, Cambridge cb2 2ru, UK
Published in the United States of America by Cambridge University Press, New York
www.cambridge.org
Information on this title: www.cambridge.org/9780521247429

© Sidney Ochs 2004

This publication is in copyright. Subject to statutory exception and to the provision of

relevant collective licensing agreements, no reproduction of any part may take place
without the written permission of Cambridge University Press.

First published in print format 2004

isbn-13 978-0-511-21031-0 eBook (EBL)

isbn-10 0-511-21387-5 eBook (EBL)

isbn-13 978-0-521-24742-9 hardback

isbn-10 0-521-24742-x hardback

Cambridge University Press has no responsibility for the persistence or accuracy of urls
for external or third-party internet websites referred to in this publication, and does not
guarantee that any content on such websites is, or will remain, accurate or appropriate.
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CONTENTS

Preface page vii

1 Introduction: Greek Science and the Recognition of Nerve as
a Channel 1
2 Galen’s Physiology of the Nervous System 24
3 Nerve, Brain, and Soul in the Middle Ages 36
4 Renaissance and the New Physiology 50
5 New Physical and Chemical Models of Nerve in the
Enlightenment 63
6 New Systematizations of Nerve Function in the
Enlightenment 93
7 Electricity as the Agent of Nerve Action 108
8 Nerve Fiber Form and Transformation 130
9 Wallerian Degeneration: Early and Late Phases 169
10 Nerve Regeneration 187
11 Characterization of Axoplasmic Transport 215
12 Molecular Models of Transport 263
13 Actions of Neurotoxins and Neuropathic Changes Related to
Transport 284
14 Purposeful Reflexes and Instinctive Behavior 305
15 Neural Events Related to Learning and Memory 317
16 Epilogue: With Observations on the Relation of the Nervous
System to Mind 353

Bibliography 367
Index 421

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PREFACE

Within the last half of the twentieth century, two fundamental properties
of nerve were established: in midcentury, the ionic nature of the propagated
action potential; and, later in the century, the process in the fibers known
as axonal flow, axoplasmic transport, axonal transport, neuroplasmic transport,
and so on. By means of the transport mechanism, essential components
synthesized in the nerve cell bodies are carried out within the relatively
long length of nerve fibers to maintain their viability and function. Com-
ponents transported include the ion channels and ion pumps needed to
maintain membrane potentials all along the length of the fibers, metabolic
and structural components supporting the form and viability of the fibers,
and substances providing for reception at sensory terminals and neurotrans-
mitters at motor terminals. This is indeed a protean mechanism, fundamen-
tal for an understanding of modern neuroscience and a rational basis for
interpretation of neuropathies and eventually their therapy.
Although the discovery of the properties and molecular nature of the
transport mechanism and related topics is a major theme, this account is
not restricted to the last half century. The concept can be traced back to its
earliest beginnings in the sixth and fifth centuries B.C., respectively, when
philosophy and science had their origins in ancient Greece. Nerves were
then conceived of as channels carrying sensory impressions by animal spir-
its to the brain where consciousness awareness and reasoned judgment were
located, and from it willed commands were carried by nerves to actuate the
muscles. (Notable exceptions to the concept that the brain played this role
were Aristotle and the Stoics, who viewed the heart as serving those higher
functions.) From ancient Greece, as step-by-step physiological and anatom-
ical sciences evolved and new physical principles and chemical substances
were discovered over the centuries, various agents were proposed to replace
animal spirits without prevailing, until, in the nineteenth century, the elec-
trical nature of the nerve impulse was established and, later in the century,
the elementary unit of the nervous system, the neuron, was recognized.

vii
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viii PREFACE

In the last half of the twentieth century, electron microscopy revealed the
fine structure of the nerve fiber and isotope tracers, and biochemical tech-
niques were used to characterize the movement of proteins and other mate-
rials in them and reveal the molecular nature of the transport mechanism.
The same processes discovered in peripheral nerves were also found to take
place in the neurons of the central nervous system, where transport in the
brain was seen as underlying neuronal changes related to higher behavior,
to learning and memory. Thus, a close connection can be traced from the
earliest conceptions of nerve as a channel for an agency responsible for
sensation carried to and motor responses from to the brain.
Whereas this history makes a case for the similarity of the earliest concept
of nerve to its present understanding, a Whiggish view of history, the in-
terpretation that the past simply evolves in a direct progressive path to the
present is not taken. Our story includes false steps, strong personal opposi-
tions, and periods of stagnation or even regression, these setbacks overcome
with new thinking, often provided by the importation of concepts and tech-
niques from other sciences. Some account of the cultural background out of
which the science developed has been touched on, where philosophical and
religious teachings have acted to further or hinder the progress of discov-
ery. Liberal use was made of the best available scholarship to give English
translations of some of the primary sources to convey what was thought at
the time. This, it is hoped, will help avoid anachronisms, the temptation
to judge the work of our predecessors on the basis of present information
and standards. I have retained the older phraseology; and for some obsolete
words, I have supplied present-day equivalents in square brackets. Square
brackets were also used where elisions or additions were made to further
the sense of a quoted passage.
A chronological order has in general been followed for the first six chap-
ters until, by the late eighteenth century, the known properties of nerve and
the nervous system had grown to the point that keeping to a strict chrono-
logical order became cumbersome. From the seventh chapter on, a thematic
course was followed, with some aspects of the subject carried forward to our
day; the electrical nature of the nerve impulse, the form of the nerve fiber,
its degeneration and regeneration, the characteristics and molecular mech-
anisms proposed for axonal transport, agents interfering with transport and
their relationship to neuropathology, reflex responses, the relationship of
brain structures and transport to higher behavior, to learning and memory.
Some implications of those latter subjects are dealt with in a more specula-
tive manner in the last chapter, as part of the postscript.
Rather than an attempt to chronicle all aspects of nerve, the main purpose
is to give an account of those concepts thought to be most essential that are
related to transport. Even so, the large and ever-increasing body of literature
has made the problem of selection, particularly in dealing with the more
recent literature, acute. I am only too aware that, to keep within the bounds
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PREFACE ix

of a single volume, some aspects and worthwhile contributions could not

be included. My hope is that omissions in this respect may be overcome by
recourse to the copious references supplied.
Although, as far as is known to me, this is the first book-length treat-
ment of the history of nerve in which axonal transport figures in a major
way, some recent histories of neuroscience have dealt with some aspects of
transport or related topics. Clarke and O’Malley have given translations of a
number of important historical writings on nerve, brain, and spinal cord.1
The book by Clarke and Jacyna, dealing with fundamental developments
in the history of the nervous system during the first half of the nineteenth
century, contains important sections relative to transport.2 Liddell discusses
the early microscopic studies of the nerve fiber.3 Some of the earlier his-
tory of transport was briefly touched on in my book, which gives a general
exposition of axoplasmic transport up to 1982.4 Spillane’s book on nerve
has a more extensive clinical orientation.5 The histories of neuroscience by
Brazier6 and those by Finger7 provide useful background information. These
deal for the most part with the central nervous system. Important reviews
dealing directly with portions of the history of transport have been given by
Clarke,8 Rothschuh,9 and Billings10 and in collected volumes on axoplasmic
transport.11
The writing of this book was shaped by studies of peripheral nerve, spinal
cord, and brain properties carried out over a period of more than 50 years.
My interactions in those studies with colleagues, post-doctoral fellows, and
students was not limited to only the investigative work at hand, but they
acted as a stimulus to further understand the historical basis of what we
were involved with. I give my heartfelt thanks to all who shared their stud-
ies with me. I would like to express my gratitude to Ralph Waldo Gerard
who took me on as a doctoral student at the University of Chicago, and to
Anthonie van Harreveld, with whom I served as a post-doctoral Fellow at
the California Institute of Technology, who treated me as a colleague and
friend. Thanks must also go to the librarians at the Ruth Lilly Library of the
Indiana University School of Medicine who have been unfailing in their
help with difficult to obtain materials. I wish to express my thanks to Dr.
Katrina Halliday, my editor at Cambridge University Press, for her support
and to those other editors at Cambridge who through the years did not lose
faith that this book would eventuate. Last, but not least, this book would
not have been possible without the support of my wife Bess and our chil-
dren Rachel, Raymond, and Susie who each in their own way has helped in
the course of making this book.

1 (Clarke and O’Malley, 1968). 2 (Clarke and Jacyna, 1987).

3 (Liddell, 1960). 4 (Ochs, 1982). 5 (Spillane, 1981).
6 (Brazier, 1984) and (Brazier, 1988). 7 (Finger, 1994) and (Finger, 2000).
8 (Clarke, 1968) and (Clarke, 1978). 9 (Rothschuh, 1958). 10 (Billings, 1971).
11 (Weiss, 1982), and (Iqbal, 1986).
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1
INTRODUCTION: GREEK SCIENCE AND THE
RECOGNITION OF NERVE AS A CHANNEL

Before the dawn of civilization, primitive man believed, as does primitive

man today, in animism, magic, and supernatural forces to account for events
in the world he experienced.1 The powers of nature are seen when, after the
death of vegetation in winter, its rebirth occurs in spring. Storms with their
lightning and thunder, wild animals, and the unpredictable and often tur-
bulent behavior of man in relation to man were powers anthropomorphized
through the action of spirits who were either beneficent or malevolent. The
emotions felt within himself, man projected to other men, to other living
beings, and even to inanimate objects moved by unseen forces.
With the rise of Greek philosophy and science, another view of nature
and man arose: the belief that the cosmos and man are ruled by impersonal
laws, that the gods do not take a providential interest in the affairs of man.
As scientific knowledge evolved and the structures and functions of the
various body organs became recognized, the nerves were singled out as
having an integral relation to sensation and body movements. In some of
the earliest accounts of nerve, they were thought of as channels carrying
a spiritual influence to the brain in which consciousness and willed motor
control over the body was located.

THE EARLY CONCEPTION OF NERVE CONFOUNDED WITH TENDONS

The artifacts and cave drawings left by prehistoric man attest to his powers
of observation. In the course of hunting or warfare, he would have seen mus-
cles become lax and limbs made useless by the severing of large tendons. But
the tendon was not clearly identified. It could be muscle tendons (such as
those of the hamstrings) or a major nerve (such as the sciatic). In the archaic
Greek civilization represented in Homer’s epic The Iliad,2 the word neuron

1 (Frazer, 1922).
2 c. 8th century B.C., probably first written down in the sixth century.

1
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2 A HISTORY OF NERVE FUNCTIONS

was applied both to tendons and nerves, and analogized to a bowstring

taut with tension applied to it or lax when severed. The standard dictionary
definitions in use to this day attest to the order of its ancient derivation.
Under the dictionary heading of “nerve,” we find the first meanings given
are “sinew” and “tendon,” with the idea of putting forward the utmost
exertion, as to “strain every tendon.”3 The later meaning given is that it is
“cord-like or filamentous tissue connecting parts of the nervous system and
organs of the body.” It was defined in 1606 as, “A fibre or bundle of fibres
arising from the brain, spinal cord, or other ganglionic organ, capable of
stimulation by various means, and serving to convey impulses (especially
of sensation and motion) between the brain, etc., and some other part of
the body.”4 A number of other meanings given for its modern use relate
to its original meaning as a tendon, namely as subserving vitality, force,
physical strength, fortitude, vigor, endurance, and also curiously its inverse,
oversensitiveness and nervous weakness.5
In the Old Testament, reference is made to “the sinew present in the thigh”
with some confusion with blood vessels, as in the translation “the principal
vein of the leg which is in the thigh, commonly the sciatic nerve” and, to the
“sinew of the thigh-vein or thigh-nerve.” That the nerve was implicated is
indicated when, in the struggle of Jacob with a strange man (Angel or God?),
Jacob was “touched on the hollow of his thigh, which lamed him.”6 This
is why it is said that, “the Israelites to this day do not eat the sinew of the
nerve that runs in the hollow of the thigh.” From the era of the Patriarchs,
eating the flesh of that part of the leg (the rump) containing this nerve
(the sciatic) was forbidden, and this proscription was maintained as part of
Kosher law. However, the flesh may be eaten if the nerve is first removed

3 (Webster’s, 1966).
4 (Oxford, 1944). In earlier dictionaries devoted to medicine (Castelli, 1761), the latin
term nervus derived from the Greek neuron while described in relation to tendons
and ligaments, the bulk of the definition dealt with its then modern role as channels
conveying animal spirits to support sensation and motion.
5 (Oxford, 1971). Samuel Johnson gave as the first meaning for nerve an organ of
sensation, the second the use by poets for sinew and tendon, and the third for force
and strength (Johnson, 1827). It is interesting that in our time only by the eighth
definition do we find reference to nerve as a fiber or bundle of fibers arising from the
brain and acting to convey impulses of sensation or motion. Another relation of the
term nerve to tendons comes from the early experiences with stringed instruments.
The strings, when stretched, give rise to a higher note on plucking them. Thus, an
individual, if overly sensitive or nervous, is said to be high strung.
6 (Bible, 1970), Genesis 32:31–32. This is variously translated. The New English Bible
has it that a dislocation at the hip occurred. Translating the passage from the Latin
Vulgate, “He touched his (Jacob’s) nervum femoris (femoral nerve).” But, the femoral
nerve supplies the anterior surface of the thigh, and the reference is clearly to the
hollow of the thigh. Continuing, the passage reads, “immediately (the nerve or leg)
became feeble” (reading emascuit-withered or feeble).
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INTRODUCTION 3

in the process known as porging.7 The custom of porging appears to have

been carried out in an old, isolated Jewish enclave in China by the Jews who
lived in Kaifeng (K’ai-feng), the old Capital city of the province of Honan,8
where the Chinese referred to them as the T’iao-chin chiao, the people who
“pick out the tendons.”9
An analogy to the biblical injunction against eating the rump because of
the sciatic nerve within it was the practice carried out among some North
American Indian tribes of regularly cutting out and throwing away the thigh
muscles containing the nerve.10 The reason given by the Cherokee Indians
was that the “tendon,” when cut, retracts, with the muscles becoming lax;
and they did not wish to expose themselves to the danger of also becoming
weakened if they were to eat it. The notion is clearly based on sympathetic
magic.11 The struggle of Jacob in Genesis may very well also have had a simi-
lar origin in sympathetic magic that was later given a mythic interpretation.

PRIMITIVE ANIMISTIC BELIEF IN SPIRITS ANIMATING THINGS, AS

WELL AS LIVING BEINGS
An insight into the thought of the ancient man was given by the stud-
ies of aboriginal peoples in Polynesia and elsewhere in remote corners of
the world by explorers, evangelizers, and anthropologists. An extraordinary
opportunity to directly study the thinking of a primitive man came about
when in 1911 an Indian, Ishi, emerged from the foothills of a remote moun-
tain in northern California. He was the last of an isolated Stone Age tribe
that had completely died out but for him.12 Ishi was patient, cheerful,
good-natured, with the capacity to learn equal to that of modern man. He

7 (Klein, 1979).
8 Jews entered China via the Silk Road as traders in a number of places in China,
perhaps as early as during the Han dynasty (206 B.C.–220 A.D.) (White, 1966), p. 52,
though the earliest tangible evidence of their presence is around 718 with a settled
Jewish community in Kaifeng more definitely attested to by a synagogue built in
1163.
9 (White, 1966) ref. to (Lépine, 1894), Part 1, p. 51, Part 2, note 18, p. 24 and p. 110.
The term “T’iao” refers to jumping, “chin” to the tendon or nerve, the jumping
nerve, and “chiao” to a hollow, wherein by digging the sciatic nerve could be
removed from the rump and thigh muscles.
10 (Gaster, 1969), pp. 210–211. 11 Ibid., pp. 211–212.
12 (Kroeber, 1994), pp. 23, 78. Hungry, sick, and alone, Ishi came into the hands of
two California anthropologists: T. T. Waterman and Alfred L. Kroeber. With the
assistance of an Indian from a bordering Indian tribe who had a dialect close to
that of the Indian and the linguist Edward Sapir, he was able to communicate the
story of his life. Ichi was a Stone Age man who had stepped out of the remote
shadows of the past. He lived on for four plus years of his life quartered in the
museum transmitting his language and culture. He demonstrated how he made
obsidian knives and arrowheads, bows and arrows. He also fished and hunted.
While housed in a hospital, Ishi witnessed a number of surgeries. These did not
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