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.

References

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