HowWe Control the Contraction of Out Muscles -

VolZllltar,r lnZlsclilar movements are driven by a servomechanism similar

In

many respects to the alitOlnatic feedback systeln

employed to control po(ver-assisted steering zn

an

automobile

by P. A. Merton

P

sychophysics is the branch of ex­

because physiologists for metaphysical

perimental science that deals with

reasons feel that conscious volition is a

few definite phenomena to describe.

the

faintly disreputable thing for them to

With them we reach a new point of

relation

between

conscious

mental events and physical events with­

have dealings with.

tentious, as titles will be. There are a

view, from which I hope we can see a

in and without the body. Most psycho­

In sensory psychophysics it is easy

physics is sensory psychophysics, which

to find illustrative examples of sensory

simple movements and not come close to

deals with the relation between a physi­

phenomena that have an analytical char­

explaining the individuality of hand­

cal stimulus and the resulting sensation

acter, that is, examples that provide

writing. (That subject was introduced

experienced

by the subject. The ob­

some insight· into sensory mechanisms,

partly to advertise the fact that sensory

ject of sensory-psychophysical experi­

but on the motor side it is not so easy.

physiologists do not have all the glamor

ments is to gain understanding of the

I can think of one striking instance. A

problems. ) It will be useful to start by

phYSiological mechanisms that lie be­

motor psychophysical fact of immense

drawing an analogy between the human

tween the stimulus and the sensation,

everyday importance is the individuality

body and an automobile.

and to be able to draw inferences about

of a person's signature. Whenever Mr.

In the old days the steering wheel

what goes on inside a sense organ, a

X makes the appropriate volitional ef­

of a motorcar was directly connected to

Measurements of

fort and signs his name, it always comes

the road

subjective sensory thresholds in any sen­

out the same (or enough so to be recog­

and linkages, and the brake pedal simi­

sory mode (tactile, visual, auditory or

nizable) and different from what any­

larly applied pressure directly to the

whatever), perceptions of color matches

one can write if he tries to write the

brake shoes. On coming to a hill a gear­

and judgments of the pitch of a note or

same name. This is not an analytical

shift could be moved to engage a suit­ able pair of gears to climb the hill with.

nerve or the brain.

general line of advance. I shall stick to

w heels

by a series of levers

the direction of a sound are examples

observation; it is just a mysterious phys­

of sensory-psychophysical observations.

iological fact, which we take for granted

Today, in order to enable the driver,

Sensory psychophysics is an old and

because we are so familiar with it. What

no matter how frail, to control a massive

highly respectable subject. In the hands

does tell us something, however, is the

vehicle with the Rick of a wrist or ankle,

of such investigators as Thomas Young,

further observation that if Mr. X takes

sophisticated mechanisms have been de­

Jan Purkinje, Hermann von Helmholtz,

a piece of chalk and signs his name in

veloped to assist with steering, brakin g

James Clerk Maxwell,

Lord Rayleigh

large letters on a blackboard, it again

and gear-shifting. All these mechanisms

and their modern successors it has told

comes out the same. The muscles used

have devices (sensors, we may·call them)

us a great deal about vision, hearing and

are different but the individuality re­

that measure some physical variable (for

other senses. Young's celebrated three­

mains. From this observation we learn

example brake pressure or engine revolu­

color theory of color vision, published

something about the organization of the

tions) and use the "feedback" informa­

in 1802, was formulated entirely on psy­

motor system.

tion from them to control the mechanism

chophYSical evidence and is the basis of modern color photography and color television.

that assists the driver. Let us concen­

I

n

this

article

evidence

from

both

trate on the mechanism that assists with

branches of psychophysics is taken

steering. In its essentials it works as fol­

into account, but the main object is to re­

lows. Each position of the steering wheel

have

dress the balance in favor of the motor

corresponds to a certain angle of the

these credentials. It deals with the re­

side. In more concrete terms we ask:

front road wheels that the driver would

ciprocal problem, the relation between a

What has been learned by making ob­

like them to assume with respect to the

conscious effort of will and the resulting

servations on voluntary movements in

fore-and-aft axis of the chassis. A sensor

physical movement of the blldy. It is just

man about the phYSiological mechanisms

at the bottom of the steering column de­

as important to know how we move as

that make our muscles do what we ex­

tects the difference between this "de­

how we feel, but on the motor side much

pect of them? Not, of course, vel'y much.

manded" pOSition and the actual posi­

less has been achieved, partly, I suspect,

The title of this article is somewhat pre-

tion of the road wheels. Signals from

The other branch of psychophysics, motor

psychophysics,

does

not

30

© 1972 SCIENTIFIC AMERICAN, INC

MOTOR NERVE TRUNK

SENSORY FIBER FROM MUSCLE SPINDLE

MOTOR FIBER TO INTRAFUSAL MUSCLE

NERVE BUNDLE TO MUSCLE SPINDLE

PRIMARY ENDING --':"'-c-:'--1!!!!l� SENSORY NERVE FIBER FROM TENDON ORGAN

INTRAFUSAL MUSCLE FIBER

TENDON "",,-,..,,, ::;-- ORGAN

ARRANGEMENT OF SENSE ORGANS in a typical muscle is in·

ry nerve. In the equatorial region the cross striations, which al

d ieated in these simplified diagrams. The proportions in the dia.

an indication of the presence of a contractile mechanism within tI

gram at left are highly distorted. A real muscle fiber is only about

fiber, are absent. Hence when the intrafusal fibers contract, this

tenth of a millimeter in diameter, but it is often several centime·

region is extended and excites the sensory endings, just as if tbe

a

ters long. A muscle spiridle is somewhafthinner; if consists of even

region had been extended by stretching the entire muscle and the

finer specialized structures called intrafusal muscle fibers. Only

spindle within it. In this diagram only two intrafusal fibers are

two ordinary muscle fibers and one spindle are depicted in detail;

shown; a real spindle often has half a dozen or more. Moreover, in·

real muscle may contain tens of thousands of muscle fibers and

trafusal fibers come in two distinct varieties, only one of which is

a

hundreds of spindles. The diagram at right gives an enlarged view

shown here. Another complication is the lact that there are three

of the equatorial region of a muscle spindle. Wrapped around the

distinct kinds of motor nerve to the intrafusal fibers. In a real

intrafusal muscle fibers are the terminations of the sensory nerve

spindle the equatorial region is also much longer than depicted

fiber; the lunction of these sense endings is to respond to mechani·

here. Photomicrographs showing the innervation of a tendon organ

cal deformation by causing nerve impulses to be sent up the senso·

and the equatorial region of a muscle spindle appear on page 34.

31

© 1972 SCIENTIFIC AMERICAN, INC

tion of tension and length? Sometimes

the sensor, called the misalignment de­

and the output of the heart are con­

tector, are used to turn on a small servo­

trolled so as to suit the current needs

tension and sometimes length? Now we

motor (from the Latin

meaning

of the body; we are quite unaware of

see the nature of the problem. It is the

slave), which turns the road wheels in

the functioning of these systems and

inverse of the automobile designer's. We

such a direction as to cancel the mis­

of the signals from the pressure sensors

are presented with the sensors and we

alignment. Thus the road wheels are

in the walls of the arteries and else­

have to discover what the mechanism

made to point in the direction the driv­

where that are a part of them.

they are part of was designed to do.

servus,

er wants, without his having to exert

Such mechanisms are commonplace

What precisely do we ask of our muscles

himself. As he turns the steering wheel

physiology; they are in the textbooks

that they need these confidential sen­

for medical students and nurses. When

sors to make them do it? It is by no

Such is power-assisted steering. An

we come to muscle, however, the situa­

means obvious.

engineer calls it a follow-up servomech­

tion is different. To return to our anal­

Having thus briefly sketched the pic­

anism. An important point to note is

ogy, in the case of the automobile we

ture, let me now go into the physiology

that, the function of the device being

know what we want to control-direc­

in more detail. It falls into two sections.

to help the driver automatically, he does

tion, speed or retardation-and the prob­

The first presents the evidence that mus­

not want to be bothered with the de­

lem is to design servomechanisms to

cles incorporate sensory

tails of its operation; in particular he

help the driver, with appropriate sen­

whose signals we are not consciously

the road wheels follow automatically.

receptors of

would only be distracted from his task

sors in each instance. The signals from

aware;

of keeping his eyes on the road to see

the sensors are just part of the engi­

known of the mechanisms in which they

the second discusses what is

where to steer if signals from the sensor

neering technology, and so we do not

take part.

were relayed to him. They give informa­

display them on dials on the dashboard.

tion that is relevant only to the func­

They would only put the driver off. In

tioning of what ought to be a completely

the human machine we have muscles to

I

subservient mechanism, and they should

control. How do we do it? Do the or­

tablished for the first time that the in­

remain private to that mechanism.

ders to contract go directly from the

ternal organs of the body, such as the

brain? Presumably not, since on exami­

heart, the stomach and the brain, are in general insensitive to the kind of stimuli

Power-assisted steering relieves the

n

the 18th century the great Swiss

physiologist Albrecht von Haller es­

driver of physical effort only; other such

nation it appears that muscles, like the

devices relieve him of mental effort too.

automobile, are equipped with sensors

that are so readily felt by the skin: prick­

The automatic transmission, for exam­

of their own, of whose signals the own­

ing, pinching, cutting, burning and so

ple, does away with the need to decide

er of the muscles, like the owner of the

forth. It is this fact that enables surgeons

when to change gear, as well as the need

automobile, remains unaware. Presum­

to perform operations on, say, the brain

to perform the change. In an aircraft

ably, like the sensors in the automobile,

substance with only

the automatic pilot does everything and

they are taking part in automatic mech­

around the incision. In his studies of

leaves the human pilot completely free.

anisms that assist the subject in con­

muscle Haller found that stretching a

trolling his muscles. What are they help­

muscle by pulling gently on the tendon exposed in a wound in a human sub­

In the human body there are numer­

local

anesthesia

ous automatic feedback mechanisms of

ing to control? Muscle tension perhaps?

this kind controlling physiological func­

It could be; some of them measure ten­

ject did not cause sensations of either

tions without any mental effort on our

sion. Length? Others of them respond to

movement

part. For instance, the blood pressure

changes in muscle length. A combina-

however, is painful.) Reflecting on Hal­

or

tension.

(Pulling

hard,

ler's observations, one can perceive that the viscera and the muscles are really in different categories. It is not at all

I tv �+

��

t.1v,

�K.d

�

�f

surprising, when one comes to think of it, that the liver should be insensitive to cutting with a knife or burning with a cigarette; such stimuli would be so

� � �k-t.!;

Yt-v.... � S

rare

without the animal's getting an

earlier and more effective warning from the abdominal skin that to develop a system to report them would give the animal a negligible evolutionary advan­

�

��

�f !Lt

V-�,{

�

IMvtW.���

� ��'f

tage, whereas sensitivity to mechanical contacts, which the skin preeminently possesses, would very likely be a positive disadvantage. Imagine what life would be like if throughout it one were as viv­ idly aware of the beat of one's heart as the surgeon who puts a finger on it exposed during an operation! With mus­

STRIKING EXAMPLE of a simple experimental observation that provides some insight into the organization of the motor psychophysical system is represented by these two hand· written versions of a sentence taken from the text of this article. The sentence was written large on a wall with a felt·tipped pen (top) and small on a piece of paper with a fine map· ping pen (bottom). The writing on the wall is about 10 times larger. The large writing was

cle, however, it is quite otherwise. It might be useful for us to be conscious of how extended our muscles are at any moment, since that determines the po­ sition of our limbs, and also to know

done by movements of the wrist, elbow and shoulder, whereas the small writing used mus·

their rate of shortening or elongation

cles in the hand itself. Nevertheless, the character of the writing is the same in both cases.

and the tension in them. If we are to be-

32

© 1972 SCIENTIFIC AMERICAN, INC

lieve Haller, this is just what they do not tell us. For this and other reasons that will shortly emerge we find that, where­ as the insentience of the viscera has long been received as physiological dogma with a status comparable to the circula­ tion of the blood, the insentience of mus­ cle has often been called in question and probably cannot be regarded as univer­ sally accepted even today. For me the question was both raised and answered the day I read the argu­ ments of Helmholtz, published in 1867 in his

Handbook of Physiological Optics.

Helmholtz reached the same conclusion as Haller by experiments with the eye, which have the merit that anyone can repeat them and convince himself of the facts. Helmholtz starts with the fa­ miliar observation that if one takes hold of the skin at the outer corner of the eyelids and jerks it sideways, the eye itself is moved and what one sees with that eye appears to jump about. On the other hand, we know that if one moves one's eyes voluntarily, the scene one is looking at does not appear to jump. Helmholtz argues as follows. In both cases the image of the external world moves over the retina as the eye moves. When one moves one's eyes actively, by voluntary effort, one allows for the eye movement and does not interpret the movement of the image on the retina as signifying a movement of the ex­ ternal world. When the eyes are moved passively by an external pull, however, one interprets what one sees as if the eye had remained still. The movement of the image on the retina is assumed to be due to a movement of the external world and not to a movement of the eye. Hence we only know in which direction our eyes are pointing when we move them voluntarily, and this must be be­ cause we make an unconscious estimate of the effort put into moving them. (We have a "sense of effort.") Sense organs in the eye muscles (or elsewhere around the eye, if there are any) do not tell us which way our eyes are pointing, be­ cause when the eyes are moved passive­

INSENTIENCE OF EYE MUSCLES was demonstrated a few years ago by means of an in· genious experiment devised by G. S. Brindley, now at the Maudsley Hospital in London. In these photographs, made in the course of the experiment, Brindley is manipulating the author's eye with forceps to test whether, after blinding it with a black cap, there was any awareness of passive movements. There was not. The white spot on the cap is to give an indication of eye position. The eye and the lids were treated with local anesthetic.

ly, we do not seem to know they have moved. This argument, as it stands, is not

This objection, as Helmholtz argues,

conclusive, because when the eyelids

can be answered by considering after­

No matter how hard one pulls on the

are pulled, the sense organs in the eye

images. If one stares fixedly at a bright

eyelids the afterimage appears to re­

movements quite the opposite is found.

muscles or elsewhere might not be ex­

light for 15 to 30 seconds (please, not

main completely stationary.

cited in the same manner as when the

the sun!), then on looking elsewhere

to be certain of this phenomenon it is

eye is turned normally by the contrac­

an afterimage of the bright light is per­

necessary to view the afterimage against

tion of its muscles. The apparent move­

ceived and persists for a minute or so.

a featureless background,

ment of the external world during a

When an object is fixated steadily, the

sheet of plain paper held close to the

passive movement of the eye

In order

such as a

might

afterimage likewise stays still, but when

eye; otherwise the concomitant apparent

therefore be due to a misjudgment of

the gaze is shifted, the afterimage also

jerking around of external objects may

the eye's direction rather than to a com­

moves. This, of course, refers to active

make the judgment difficult. Hence dur­

plete ignorance of its movement.

voluntary eye movements.

ing

In passive

passive

movements

we

interpret

33

© 1972 SCIENTIFIC AMERICAN, INC

we are looking, but only because an in­

what we see precisely as if tbe eye had

ous quantities of local-anesthetic eye

not moved at all. It is not a matter of a

drops.) The test proved that subjects are

ternal "sense of effort" gives us an esti­

quantitative misjudgment. The reader

quite unaware of large passive rotations

mate of how much we have exerted our

is encouraged to repeat for himself these

of the eye in its socket of 30 degrees or

eye muscles.

crucial observations and reflect on the

more; they do not know the eye is being

are artificially impeded, or if passive

compelling conclusions Helmholtz drew

manipulated at all unless the forceps

movements are imposed, we absolutely

from them.

happen to touch the eyelid. Another im­

do not know what is going on-unless

If voluntary movements

portant point was that if the subject was

we can see and reason back from the visual illusions we receive.

A- - ley (now at the Maudsley Hospital

invited to voluntarily move his eyeball while the forceps were gripping it, he

So much for the eyes. In the limbs

in London), who has a genius for set­

was unable to tell whether the experi­

the same facts are less easily demon­

tling or eliminating argument by incisive

menter holding the forceps was allowing

strated. To use Haller's method with

experiment, proposed that we confirm

the movement to take place or was pre­

patients whose tendons have ,been ex­

Helmholtz directly by blinding an eye

venting the eye from moving.

posed

few years ago my friend C. S. Brind-

with a black cap on the cornea ( the eye's

The

unequivocal conclusion

of

all

under

local

anesthetic

in the

course of an orthopedic operation is one

transparent front surface) and then mov­

these experiments is that we have no

possibility, but it does not satisfy the

ing the eye around with forceps to see if

sense organs in the eye muscles or near

powerful compulsion that all investiga­

the subject could feel the movement.

them that tell us which way our eyes are

tors in sensory physiology have to try it

(Pain was prevented by instilling gener-

pointing. We normally know which way

for themselves. A paper on visual illu­ sions in which the author had not ex­ perienced the phenomena himself is al­ most unthinkable, and rightly so. What better way could he have of satisfying himself that they were correctly report­ ed? Hence it is desirable to find a meth­ od for studying muscular sensibility in ordinary limb muscles of healthy sub­ jects. The difficulty, of course, is to de­ vise a way of stretching a muscle with­ out the subject's knowing what is being done, since he can feel pressure on the skin or the movement of a jOint. Local anesthesia of an extremity provides an answer. Investigators have variously in­

TENDON ORGAN contains sense endings that signal to the nervous system the tension in the part of the muscle in which they lie. A typical location of a tendon organ is shown in the diagram on page 31. The single sensory nerve fiber that services the tendon organ has been made to appear black in this photograph by means of a special silver stain. The nerve fiber divides many times, terminating in very fine branches with knobs at the ends. These

jected local anesthetic around the joint at the base of the big toe or at the base of a finger, or have anesthetized the entire hand by cutting off the blood sup­ ply with a pneumatic tourniquet around

structures, in some unknown way, sense the deformation produced by tension and cause

the wrist for about 90 minutes. Move­

nerve impulses to be sent up the sensory fiber at a rate that is determined by the tension.

ment

This tendon organ was dissected out of the leg muscle of a cat; it is about half a millimeter

stretches

long. Surrounding one end are the remains of muscle fibers. Both photographs on this page

which lie above the anesthetized region.

were made by Colin Smith, Michael Stacey and David Barker of the University of Durham.

of

an the

anesthetized muscles

that

digit

then

move

it,

My collaborators and I use the top jOint of the thumb, which has the advantage that only one muscle (lying well up in the forearm) flexes it, whereas the joints of the fingers are operated by more than one muscle, some in the hand and some in the forearm. Thus when the thumb is anesthetized by a tourniquet at the wrist, voluntary movements of the top jOint are unimpaired in strength. We have also used injection of local an­ esthetic around the base of the thumb. The uniform result of numerous ex­ periments is that, with an adequate depth of anesthesia, the subject (whose eyes are shut) cannot tell in what posi­

E Q UATORIAL REGION of a muscle spindle dissected from the leg muscle of a rabbit ap­ pears in this photomicrograph; the part shown is about a millimeter long. Again the nerve fibers and nerve endings have been stained with a silver stain, making it possible to distin·

tion the experimenter is holding the top of his thumb, or whether he is bending it backward and forward. This is true

guish clearly the equatorial capsule, the intrafusal muscle fibers and the sensory endings

only provided that the movement is not

wrapped around them. The nerve ending to the right is a primary ending; its sensory

rapid and that the thumb is not forcibly

nerve fiber enters from lower right. The other ending is a secondary ending; its nerve fiber

extended or flexed at the limits of its

enters from upper right. The finer nerve fibers are part of the motor nervous system.

range of movement. It is also the case

34 © 1972 SCIENTIFIC AMERICAN, INC

SPINAL CORD

3

2

1

MUSCLE SPINDLE

t ...-

STRETCH REFLEX is mediated by t he nervous ollceha"i,,,, tie·

o,.,.uw

picted in this highly schematic illustration. A muscle is under the

excite it. As a result motor impulses are sent back down to the

influence of the stretch reflex when it is engaged in a steady con·

muscle (downward arrow), where they cause it to contract (3).

traction of a voluntary nature, as when

More complicated nervous pathways than the one shown may also

a

person's elbow is flexed

),

wbeloe they illlPinge on a Illotor

n er v e

eell

at a synapse and

steadily against a load (1). A sudden unexpected increase in the

be involved in the stretch reflex. Any real muscle is, of course, sup·

load (2) stretches the muscle, causing the sense ending on the

plied with many motor nerve fibers and spindles. In addition the

muscle spindle to send nerve impulses to the spinal cord (uJJward

synaptic connections to even a single motor nerve cell are multiple.

that if the subject attempts to flex his

of sense organs, and very fine sense or­

thumb, he cannot tell whether he has

gans at that. The principal kind, the

(between, one might say, the different

been successful, or whether the experi­

muscle spindles, are the most elaborate

types of information required by the

menter has prevented it from moving.

sensory structures in the body outside

legislature and the executive). He al­

Thus with skin and joint sensation elim­

of the eyes and ears. This deep paradox

lowed

inated the thumb behaves jus t like the

(for which the reader has already been

Helmholtz had been wrong and that

prepared) is at the back of everything

his own discovery showed that muscles

in this article. AIl.the essential facts that

were sentient after all.

eye. Muscle is insentient.

that enables him to do so effortlessly

himself to be persuaded that

have already argued that onc would

create it have been known since 1894,

Sherrington had thus taken the view

on general grounds expect the

when Sir Charles Shenington proved

that in effect there was no paradox, and

liver, say, to have sensibility like the

conclusively that there were nerve fibers

his influence was so immense that it was

skin's. Indeed, if one looks at the liver

going to the muscle spindles that be­

60 years before the true situation was

through a microscope, it has none of the

longed to the body's system of sensory

at last clearly perceived. By this time

I not

elaborate apparatus of sensibility seen

nerves, and hence established that the

the paradox had much less impact, since

in the skin-no network of branching

muscle spindles were sense organs. Un­

physiologists had discovered many of the facts about the muscle spindle need­

nerve fibers ending in a variety of char­

fortunately in those distant days Sher­

acteristic sensitive structures: the sense

rin gton was insensitive to the class dis­

ed for its resolution. Before going on to

organs. The same goes for other viscera.

tinction between the information on the

these facts I should finish the present story.

Muscles are not so obliging. They arc

road sign that tells the driver to turn

supposed to be insentient, but when wc

right and the information from the sen­

look inside them, they turn out to be full

sors in his power-assisted steering gear

In the past few years the paradox has been

given

a

further

twist.

Several

35

© 1972 SCIENTIFIC AMERICAN, INC

groups of workers on both sides of the

from the skin (or for that matter from

rington in 1894, but it still remains one

Atlantic, whose members are too numer­

the eyes or ears) they cannot be used to

of the most challenging observations in

ous to name individually, have found

set up a conditioned reflex. Without ex­

the physiology of the motor system;

that signals from muscle sense organs

plaining what is meant by this fact in

even if the interpretations to be put for­

find their way to the cerebral cortex. It

detail one can say that it strongly sug­

ward later in this article are on the

seems that they get to the cortex but

gests the cat is not conscious of the sig­

right lines, it is most improbable that

we remain unconscious of them. This is

nals from its muscles.

very surprising. No one imagines for a

they are more than one facet of the

The first part of this aIticle was in­

moment that we do not make use of all

tended to introduce the reader to the

the information our eyes send to the

idea that muscle organs function at a

truth. Muscle

spindles

(they

are

called

spindles because they are long and thin

cerebral cortcx to build up the picture

subconscious level in a purely subservi­

and have pointed ends) consist of a bun­

of the outside world we consciously per­

ent role. Like the perfect servant, they

dle of modified muscle fibers, the intra­

ceive, and I am sure that a few years

work so unobtrusively that we are un­

fusal muscle fibers (from the Latin fu­

ago any

would

conscious of them, but the findings about

sus, meaning spindle), with the sensory

have been prepared to extend this point

cortical projection begin to strain the

nerve fibers wrapped around a short

of view to sensory information of any

analogy.

The

specialized region somewhere near the

kind that could be shown to get to the

scientist

Henry

Cavendish reportedly

middle of their length. The stimulus that

cortex.

dismissed any servant he caught sight

excites a muscle spindle is the stretch­ ing of this specialized sensory region.

ordinary

physiologist

eccentric

18th-century

The evidence for what I have just

of. He wrote down what food he wanted

said is not complete. The animal most

and it was put out for him. It would have

Now, as I have said, the muscle spindles

resembling man in which signals from

been going too far to expect the butler

are contractile. They are not, however,

muscle sense organs have been shown

to wait on him at table without betray­

equally contractile along their entire

to reach the cortex is the baboon. It

ing his presence, but that is what the

length; the contractile apparatus fades

seems unlikely that they do not reach

muscle sense organs seem to manage to

out in the sensory region, and the middle

the cortex in man, and equally unlikely

do!

of the sensory region, where the sense

that a baboon should be conscious of the Signals from its muscles when a man

endings connected to the largest nerve carcely less remarkable than the mere

fibers lie, probably does not contract at

is not. A strong hint also comes from the

S existence

of the muscle spindles is

all. When the spindle contracts, these

cat. John E. Swett and C. M. Bourassa of

the fact that they (the most important

sense endings (known as the primary

the Upstate Medical Center of the State

of the two kinds of muscle sense organ)

endings) are stretched by the contraction

University of New York showed that

are themselves contractile.

muscle sense organs send signals to the

unique propelty among sensory struc­

cat's cerebral cortex, but unlike signals

tures. That was perfectly clear to Sher-

1

FROM BRAIN

This is a

of the remainder of the spindle and dis­ charge nerve impulses. The next pOint to observe is that the

3

2

MUSCLE SPINDLE

SERVOMECHANISM involved in the control of voluntary mus·

transmitted along this special fiber (2), the spindle contracts, excit·

cular contractions is shown here. The basic diagram (1) is the

ing the spindle sensory ending, just as if the spindle had been

same as it is in the illustration of the stretch reflex, but with pro·

stretched. Consequently a contraction of the main muscle is excited

vision made for signals from the brain to cause the muscle spindle

by way of the stretch·reflex pathway (3, 4). In a real muscle this

to contract by way of a special motor nerve fiber. When a signal is

picture is further complicated by the existence of a direct pathway

36

© 1972 SCIENTIFIC AMERICAN, INC

muscle spindles lie among the ordinary

the next question is: "Vhat do these im­

length of the muscles to be kept roughly

muscle

red

pulses do when they reach the central

constant so that posture is maintained.

stringy structures, visible to the unaided

nervous system? Their best-established

The stretch reflex can achieve this result

eye, that actually do the work) and share

function is to excite an automatic con­

for the horse because it is based on a

their attachments to bone or tendon.

traction-the stretch reflex-in the muscle

sensor-the muscle spindle-that mea­

Hence they change length as the main

from which they come. This they do, at

sures length, or, to be more exact, differ­

muscle fibers change length. If a con­

least in part, by impinging directly on

ences in length.

traction of a muscle spindle, which ex­

those nerve cells in the spinal cord that

fibers

(the

much

larger

cites its primary ending, is succeeded by

give rise to the motor nerve fibers to the

an equal contraction of the main muscle,

muscle in question.

hat happens when it is desired that

W the muscles should execute a move­

the stretch will be taken off the sensory

The most familiar manifestation of

ment, not merely maintain a stationary

region and the ending will be silenced.

the stretch reflex is the knee jerk, widely

posture or some other steady contrac­

The spindle primary, in fact, is sensitive

used in medicine to test the state of the

tion? The obvious trick is to cause the

to the difference in length between the

nervous pathways concerned. A physi­

spindles to contract at the desired rate

spindle and the main muscle fibers; it is

cian strikes the tendon below the knee­

so that the sensory endings on the spin­

a misalignment detector. It discharges if

cap with a rubber hammer, and in a

dles will be excited if the main muscle

contraction of the spindle is not matched

healthy subject the muscles that straight­

does not itself keep up with the spindles,

by contraction of the main muscle, or,

en the knee briefly contract involun­

that is, does not contract at the desired

vice versa, if extension of the main mus­

tarily. The effect of striking the tendon

rate. In this way the advantages of auto­

cle is not accompanied by relaxation of

is slightly and suddenly to stretch these

matic compensation for changes of load

the spindle. There is no obligation for

muscles, and so to excite their muscle

by means of the stretch reflex could be

the muscle spindles and the main muscle

spindles. The tendon itself has no part in

retained during active shortening. Con­

to contract and relax together, because

the sensory mechanism. The tendon jerk

traction of the spindles would in effect

the motor nerve fibers that run to them

is quite transient, but under suitable

drive the main muscle by means of the

and carry the nerve impulses from the

circumstances a slower, sustained exten­

stretch reflex, turning on more contrac­

central nervous system that cause them

sion of a muscle will result in a sustained

tion if an unexpected obstruction were

to contract are largely separate. The

reflex contraction. If the reaction in a

met with, or if the rate of shortening for

spindles could therefore be activated

patient who is otherwise relaxed is ex­

any other reason fell behind, and, vice

while the main muscle remained pas­

aggerated, the limb is said to be "spas­

versa, damping down contraction auto­

sive, and vice versa.

tic," that is, affected by spasm.

matically if the load unexpectedly di­

Human muscles in general can be

minished, or if for some other reason

dis­

shown to be under the influence of the

the movement undesirably accelerated.

charged by the spindle primary endings,

stretch reflex when they are engaged in

Within the past year C. D. Marsden,

Having seen the circumstances un­ der

which

nerve

impulses

are

4

steady contractions of a voluntary na­

H. B. Morton and I have obtained direct

ture. The main evidence for this is that

evidence that this kind of rapid, reflex

if a subject is invited, say, to flex his

compensation does in fact occur during

elbow steadily against a load, it is found

voluntary movements in man.

that a sudden unexpected increase in

In this mode of operation the stretch

the load, which causes his elbow to ex­

reflex, as the reader will have perceived,

tend, calls up a larger contraction of his

functions as a follow-up servomecha­

biceps muscle, and conversely a de­

nism, closely analogous to power-assist­

crease in load causes a relaxation. Elec­

ed steering in an automobile. Contrac­

that

tion of the spindle corresponds to turn­

these reactions begin so soon (within

ing the steering wheel, shortening of the

trical

recording

methods

reveal

about a twentieth of a second) that they

main muscle to turning of the road

must be automatic, reflex responses.

wheels, with the spindle sensory ending

It has been realized for half a century

acting as the misalignment detector. The

that the stretch reflex confers valuable

subject can demand of his muscles either

self-regulating properties on a muscle,

a certain limb position or a certain rate

causing it automatically to adjust to

of change of limb position, and within

changes in load, without any need for

limits (limits not yet known in quantita­

the orders that the brain sends down to

tive terms) his demands will be auto­

be altered. Everyone believes the reason

matically met by his muscle servo.

the horse does not sag at the knees when

That, in brief outline, is as far as we

Douglas Fairbanks leaps from the castle

have gone in understanding how, when

parapet onto its back is that the horse's

we make a voluntary effort, the muscle

leg muscles immediately respond to the

(broken line in diagram 4) from the brain

sense organs act at a subconscious level

extra strain by way of their stretch re­

to ensure that our muscles do what we

flexes. If this interpretation is correct,

expect of them. Many facts have had to

we have one answer to the question:

be left out and without doubt many more

What does the horse expect of its mus­

remain to be discovered. To attempt any

cles? In this situation it expects them

account at this stage requires a certain

not only to exert enough force to sup­

presumption. I can only hope that when

steering analogy this pathway corresponds

port its body weight but also to adjust

the whole truth emerges, it will prove

to a direct connection between the steering

automatically to extra weight. Clearly

to be an extension and not a contradic­

wheel and the road wheels of an automobile.

what the horse really wants is for the

tion of the story I have told here.

to the main motor nerve cells. In the power·

37

© 1972 SCIENTIFIC AMERICAN, INC