HELEN E. ROSS, Stirling/ Schottland
Sensations of Innervation - A review from
WUNDT to the present day
Introduction
The majority of experimental psychologists
today use English as their main language of scientific communication, and their
view of the history of psychology is strongly coloured by the books available
in English. Particularly influential are the books of EDWIN G. BORING: "A
History of Experimental Psychology" (1929, 1959) and "Sensation and
Perception in the History of Experimental Psychology" (1942). The
Frontispiece of the former book is a reproduction of Dr. FELIX PFEIFER's bronze
plaque of WUNDT (Slide 1)*), and it is clear that BORING regarded WUNDT as the
prime founder of experimental psychology, and held him in great respect.
Nevertheless, when he came to discuss the question of "Sensations of
Innervation" (Innervationsempfindung, Innervationsgefühl) in 1942 he
concluded that WUNDT had backed the wrong side in an issue that was now totally
dead. It is my aim in this paper to show that WUNDT's position was, after all,
substantially correct; and that the issue is still very much alive in this
centennial year. What was the issue, and why did BORING state that it was dead?
This was BORING’s summary of the
situation in 1942:
"All through the second half of the
nineteenth century there persisted confusion and controversy about the
distinction between muscular sensations and sensations of innervation. Most of
the important physiologists and psychologists of this period, including both
HELMHOLTZ and WUNDT, believed that the innervation of efferent tracts in
voluntary action establishes sensations that arise wholly within the brain and
not by way of afferent fibers from the activated muscles. These sensations of
innervation, forming the sensory conscious basis of the experience of volition
were relinquished, along with the will, only reluctantly by the psychology of
the twentieth century. In the nineteenth century it was never certain whether
an experience of effort was a muscular sensation or a sensation of
innervation." He went on to add that sensations of innervation were ousted
by the theory of the reflex, furthered by the work of SHERRINGTON: "This
theory is, moreover, physiological in that it accepts conventional physiology
and ignores introspection. Since nothing is known of the activation of sensory
centers by motor centers, there is left for the explanation of this phenomenon
only the nervous circle through the muscles - or through the eyes when the
subject's own movement becomes for him a visual stimulus.
*Copies of the photographs referred to in
the text are available from the author on request.
Such a relexo-logical picture was early
adequate to the facts. Since then the increase of knowledge about
proprioceptive reflexes, as accounting for postural, articulatory and motor
mechanisms, has fixed it firmly in psychophysiological thought. That is why
sensations of innervation went out of style after 1900."
It is true that the term "Sensations
of Innervation" has gone out of style, along with the use of introspective
evidence and philosophical enquiry into the nature of volition. Nevertheless,
research continues into the relative importance of efferent and afferent
contributions to the position sense and the sense of effort. Only the vocabulary
has changed. We now speak of "corollary discharge" (SPERRY, 1950),
"efference copy" (von HOLST, 1954) or "monitoring of command
signals" (GREGORY, 1958). The interest is not in whether the motor
innervation produces a conscious sensation (which cannot be clearly determined
by introspection), but in whether the information is used separately from
afferent information.
Before discussing the experimental
evidence, I should like to try to clarify WUNDT's theoretical position. He did
not hold that sensations of innervation were the prime source of the sense of
position or effort, but merely that they contributed to it. He wrote in the
"Grundzüge" (translation 1886):
"Nevertheless, the physiologists -
with the objective of arriving at a simplification of explanations (although in
this case they have failed) - have often attempted to derive, as much as
possible, all the sensations of movement from a single source. With this
aim they have sought firstly to reduce them to sensations of skin pressure.
Secondly they wanted to see in them specific muscular sensations which,
depending on sensitive apparatuses and on nerves situated within the muscles,
should be considered in a way as the sensations of a sixth sense, a muscular
sense. Thirdly and finally, according to another supposition, there are
sensations of innervation: they derive uniquely from the central innervation of
the motor organs, and their origin would therefore be central rather than
peripheral. One can easily see that each of these three hypotheses "on the
muscular sense" is insufficient, because none is capable of explaining the
totality of the phenomena we encounter in the domain of sensations of movement.
In short, each of these hypotheses contains, evidently, a part of the truth,
and consequently the sensations of movement, as we have shown before, are for
us composed of complex products, deriving from sensations of different
origins." This extract is fairly "hygienic", in that there is no
discussion of consciousness or volition, but merely a statement about possible
neural mechanisms in relation to the experimental evidence. The type of
evidence to which he was referring came from the position sense of the eye and
limb, and the sense of weight or effort. I shall now discuss this evidence.
The position sense of the eye
Until recently there were only two major
contending theories to account for the position sense of the eye - the Inflow
and Outflow theories (Slide 2). According to the Inflow theory (SHERRINGTON
1900, 1918), eye position is known by afferent signals from the muscles.
According to the Outflow theory (HELMHOLTZ, 1866), it is known through the
monitoring of efferent command signals to the eye muscles. Reviewers have
tended to favour Outflow theory (e.g. HOWARD & TEMPLETON, 1966; MACKAY,
1973) for two main reasons: firstly, it was claimed that there was no conscious
position sense for the eyes when they were moved passively, and that the
stretch receptors of the extraocular muscles must be non-functional (IRVINE
& LUDVIGH, 1936; BRINDLEY & MERTON, 1960); secondly, it was claimed
that when an attempt is made to move paralysed eyes, the visual world appears
to move in the direction of the intended eye movement, as though the brain had
compensated for expected retinal image movement in the opposite direction.
WUNDT himself mentioned this second piece of evidence, in the "Vorlesungen
über die Menschen- und Thierseele" (1892, trans. 1894). He wrote:
"The same thing (as with the leg) happens when it is the eye that is the
totally paralysed organ. The idea of an actual movement is connected with the
inefficient resolution to perform that movement. The result is an optical
illusion; external objects appear to have moved in the direction of the
purposed movement of the diseased eye. This apparent objective movement is
evidently a necessary consequence of the subjective illusion. If the eye had
really executed the intended movement, the images cast by external objects upon
its retina could only have retained their positions unchanged, if the objects
themselves had moved in the direction of the eye and in complete accord with
it."
Curiously, WUNDT did not take this evidence
to support a pure Outflow theory. He maintained that the sense of movement of
the eye or limb was caused by the sensations from contraction of the muscle,
and he did not believe that a resolution to move it could produce the same
sensation without the muscular component. He attempted to get round the
difficulty by an appeal to a supposed conditioning process: "We must
remember that muscle-sensations always accompany the particular volition.
Hence, whenever a volition is repeated, the appropriate muscle-sensations will
be connected with it ... They will be found along with it even in cases where
the muscle is unable to contract and so to furnish the usual sense-stimulus.
... We call them reproduced sensations and ideas. ... They will, of
course, accompany (the volitions) in cases where the influence of the will upon
the muscles is normal and effective; but there they will at once fuse with the
actual muscle-sensations occasioned by the stimulus of contraction. In other
words, their effects can only be separately followed out when, as in the
illustrations given above, partial or total muscular paralysis has disturbed or
entirely destroyed the other muscle-sensations which are peripherally
excited." This obscure and neglected theory may perhaps be considered a
forerunner of modern "hybrid" theories, in which the importance of
gamma-contingent inflow from the muscle-spindles is stressed.
"Hybrid" theorists, such as MATIN (1972) and SHEBILSKE (1977), question
the primacy of outflow because of the gamma efferent system, which modifies the
inflow from the spindles (Slides 3 & 4). Inflow is facilitated by outflow:
motor commands to the eye muscles induce neural inflow via gamma efferents
before the eye muscles have contracted. Efference is necessary only as a
catalyst for afference. Spindle afference is much reduced in the absence of
gamma efference. Inflow is probably much reduced during 'passive' or 'forced'
eye movements. Such experiments do not, therefore, tell us about the role of
inflow during normal voluntary movements. The existence of hybrid inflow means
that the evidence from passive or restrained eye movements is equivocal, and
could be taken to support inflow, outflow or both. However, the evidence itself
has been challenged, in addition to the interpretation. The lack of a passive
position sense for the eye has been challenged by SKAVENSKI (1972), using a
very precise method. Instead of using forceps, he rotated the eyes gently by
contact lenses on a 3cm stalk. He then found that there was some position
sense, though not very precise. The alleged facts about paralysis and illusory
movement have also been challenged. SIEBECK (1954) and BRINDLEY et al. (1976)
claim that with complete paralysis by curare the subject is conscious that he
is unable to move his eyes, and does not experience illusory movement. Earlier
reports may have been due to incomplete paralysis. It seems, then, that WUNDT
was basically correct in supposing that efference alone was not enough, and
that some kind of efference-contingent afference was necessary for the precise
registration of eye position.
The position sense of the limbs
The limbs differ from the eyes in having
joint receptors, in addition to muscle and tendon receptors. It is therefore
possible that the relative importance of efferent and afferent signals might be
different. For the first half of the present century it was generally believed
that signals from both muscle and joint receptors contributed to the sense of
position and movement. SHERRINGTON (1900, 1918) certainly believed this. Later,
the view developed that signals from muscle receptors do not enter
consciousness, and are used only for the reflex control of movements. One of
the reasons for this was the failure of workers in the 50s to detect evoked
potentials in the cortex on stimulating group 1 muscle afferents. However,
refinements in technique allowed later workers to find them (see review in
MATTHEWS 1972). Nevertheless it was still argued by some that the muscle
spindles could not serve both the automatic stretch reflex and the conscious
position sense (e.g. MERTON, 1964). It was also claimed that the position sense
was poor or absent when the joint and skin afferents were anaesthetized - with
the implication that muscle afferents did not contribute. Some authors argued
purely for the contribution of joint receptors, others also for the importance
of command signals; but it became the orthodox view that muscle receptors did
not contribute to kinaesthesis (ROSE & MOUNTCASTLE, 1959; MATTHEWS, 1964;
MOUNTCASTLE & DARIAN-SMITH, 1968; PHILLIPS, 1969; MERTON, 1970). Just as in
the argument about eye position, the primacy of command signals was bolstered by the supposed fact that
subjects with paralysed hands or limbs might believe they had moved them
whether or not they were successful. WUNDT believed this, writing in the
"Vorlesungen": "If a patient whose leg is completely paralysed
makes a firm resolve to move it, he may have a distinct sensation of muscular
strain, and consequently an idea that the leg has really moved. By calling in
the aid of sight he can, of course, convince himself that he has been deceived:
in the dark the illusion is complete." However, as stated in the previous
section, his explanation was based not on the sensations of innervation, but on
the muscular sensations conditioned to them. Other authors have disputed the
finding, GOODWIN et al. (1972) found that subjects with anoxic hands were aware
of obstruction, provided the attempted movement was large. Conversely, subjects
may fail to feel movements which they have actually succeeded in making
(LASZLO, 1966). When totally paralysed by curare, subjects know that they
cannot move (CAMPBELL, 1970; McCLOSKEY & TORDA, 1975). The evidence from
phantom limbs is relevant here. The fact that phantoms seem to move at will has
been taken to support the primacy of command signals. However, in most cases a
stump exists below the joint, and it is not surprising that the phantom stays
in line with the stump. The interesting case is when a phantom joint is moved
below a stump. HENDERSON and SMYTH (1948) studied 300 cases, and found that the
contraction of some muscles in the stump was necessary for the apparent
movement of the phantom limb. Command signals alone were not enough. GOODWIN,
McCLOSKEY and MATTHEWS (1972) found further evidence that the muscle receptors
contribute to the position sense. They found a distortion of the apparent
position of the arm when the biceps or triceps muscles were vibrated at 100 Hz.
They suggested that vibration-induced discharges of muscle receptors are
interpreted by the brain as due to muscle-stretch caused by joint movement.
However, they point out that muscle afferent signals are meaningless on their
own, because they vary depending on the command signals. Afferent feedback from
muscle, joint and tendon receptors must be interpreted in relation to the
efferent command signals. A hybrid theory is necessary, just as it is for the
eye.
Weight perception and the sense of effort
The perception of the weight of an object,
and the sense of effort involved in lifting it, are not the same thing. There
is a tendency towards weightconstancy despite variations in the effort required
to lift a given object (FISCHEL, 1926; ROSS, 1969 et al. 1972). Nevertheless,
there is some effect on the perception of weight when the effort is varied; so
we shall treat the two topics under the one heading. WUNDT (1894 pp. 134-6)
pointed out, like WEBER before him (1834), that active lifting gave a much
smaller Weber Fraction than passive pressure alone. WUNDT wrote:
"We discriminate the magnitude of
different weights by lifting them ... This discrimination is not made in terms
of the pressure of the weights upon the skin, but by reference to the act of
lifting ... If lifting is allowed, a difference of 1/17 can be distinguished;
while in the case of simple pressure upon the skin a difference of 1/3 is only
just noticeable. So that we possess a very accurate measure of the force and
extent of movement in the movement itself. And such a measure can have been
acquired only by aid of the sensation which accompanies muscular movement ...
(Such sensations) are probably occasioned by the pressure which the contracted
muscle exerts upon the sensory nerve-fibres contained in it. But besides these
sensations accompanying actual contraction and the cutaneous sensations of
pressure and strain which are always connected with them, there are still other
sensations involved in movement, whether executed or merely intended. Our
sensations of movement are by no means dependent solely upon the external or
internal work performed by the muscles, but are influenced also by the
intensity of the impulse to movement proceeding from the central organ in which
the motor nerves have their roots. This fact is most clearly indicated by
observations on pathological changes in muscular activity. A patient who is
partly paralysed in leg or arm, so that he can only move the limb with very
great effort, has a distinct sensation of this effort: the limb feels heavier
than it used to be, as though weighted with lead; that is to say, there is a
sensation of greater expenditure of force than before, although the work
actually done is the same or even less. For the performance of this amount of
work there is required an innervation of abnormal intensity."
The increased feeling of weight and effort
in subjects with permanent or temporary paralysis has been confirmed by HEAD
& HOLMES (1911); McCLOSKEY, EBELING & GOODWIN (1974), and GANDEVIA
& McCLOSKEY (1977). WALLER (1891) also claimed that peripheral feedback
does not provide good sensory information, since weight discrimination was much
poorer during reflex contractions than voluntary lifting. Despite this
evidence, it would be a mistake to conclude that command signals are of prime
importance in judging weight. The facts concerning the size-weight illusion (CHARPENTIER,
1891) cast some doubt on this. In this illusion, the larger of two objects of
the same weight is felt to be the lighter. This is presumably due to contrast
with the expected weight. This means that the difference-signal between
the expected weight and the peripheral feedback is an important determinant of
apparent weight (ROSS & GREGORY, 1970). According to the theory of G. E.
MÜLLER and F. SCHUMANN (1889), the illusion is due to changes in motor set
(Einstellung), a larger object being lifted too easily when the muscular effort
is set in readiness for a heavier weight. (Curiously, MÜLLER and SCHUMANN did
not think their theory supported the idea of conscious sensations of
innervation, since they supposed that the "Einstellung" acted at an
unconscious level). However, the illusion can occur with passive pressure alone,
so changes in muscular tension are not a necessary component (ROSS, 1966). A
representation to the expected weight must be registered at a central level
independently of any changes in command signals to the muscles. It seems clear
that command signals make an important contribution to the sense of effort; but
their role in the complex area of weight perception is more controversial.
Concluding remarks
There can be little doubt that both motor
command signals and afferent feedback normally contribute in an interactive
manner to the position sense of the eye and limb, and to the sense of effort
and weight. But do the efferent and afferent signals give rise to separate
conscious sensations? Here we are on less firm ground. It is not clear whether
we are dealing with an empirical or a semantic issue. It is sometimes argued
that it is not an empirical question, because introspective evidence has no
validity. This scarcely seems fair, since introspective reports are accepted
all the time by psychophysicists and others. If the majority of subjects agreed
that they had distinct sensations of innervation and distinct muscular
sensations then that would constitute incontrovertible evidence that such
sensations existed. The difficulty is simply that people's introspective reports
differ: "An appeal to our own feelings of effort does not prove one thing
or another" wrote WALLER in 1891. WUNDT seems to have thought that complex
sensations were analysable into their component parts by introspection. The
passage quoted earlier from the "Grundzüge" shows that he
thought this was true of the sense of movement. It is not clear whether he
intended this to apply to all complex sensations. If he did, he would have been
wrong. Introspective evidence shows, for example, that the sense of balance is
not subjectively analysable into vestibular, visual and postural components;
nor the sense of taste into gustatory and olfactory components. Since the
introspective evidence is of little use, we are left only with semantic
arguments. Modern philosophers would probably agree that WUNDT's use of
language was unfortunate. He committed the crime of using the same word
'sensation' (Empfindung, Gefühl) for both the end product and the components.
We perceive the state of the world, and the state of our bodies, but we do not
perceive or sense our nerves firing. We may be aware of certain tingling
sensations in our muscles when moving our limbs or lifting weights, but any
such sensations are incidental to our perception of position and weight. It is
quite possible, logically, that muscular information could contribute to
perception without ever entering consciousness on its own.
A second semantic issue concerns whether
'volition' should be described as a sensation. We certainly know whether or not
we intended to move our limbs; and some people may report a 'Sensation of
Innervation' accompanying such knowledge. But it is possible to have the
knowledge without the sensation, so the two are not equivalent. We do not
usually use the language of 'sensation' to describe 'knowledge', and it seems
inappropriate to attempt to do so in this case.
We may conclude, then, that BORING'S account of 'Sensations of
Innervation' needs updating. WUNDT may not have been correct in every
particular, and his choice of language may not always have been felicitous; but
recent research has upheld his multi-component view of the position sense and
the sense of effort.
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