Brain/Volume 31/Part 3/A Human Experiment in Nerve Division/Chapter 3

by W. H. R. Rivers and Henry Head

Chapter III.—The Phenomena of Deep Sensibility.

That the muscles were endowed with sensory nerves was a necessary corollary to the universal acceptance of a "muscle sense." But Sherrington was the first to demonstrate afferent fibres in the nerves of skeletal muscles. By degenerative methods he traced their course to the muscles, and, in the opposite direction, showed that they entered the spinal cord by the posterior roots of those segments which gave rise to the motor fibres of the same muscles. This discovery did not receive the attention which was due to it, because it seemed to be little more than the last stone necessary to support the universally accepted hypothesis of "muscular sense."

But we long ago suspected that the existence of so many afferent fibres in the muscular nerves was not connected with the power of estimating movement only.

At the beginning of their investigation, Head and Sherren were brought face to face with the problem of "deep sensibility." They found, when all the cutaneous sensory nerves to a part were divided, that it was not of necessity totally anæsthetic. But, although they saw that the only structures which could account for the existence of this sensibility were the afferent fibres in the nerves of the muscles and tendons, accidental lesions of nerve trunks gave little opportunity for bringing this question to a direct issue. Accidental lesions usually divide mixed nerves containing both the fibres to the skin and to the muscles. By chance it may happen that one group has regenerated whilst the other group remains divided (as in Case 28, p. 321, Head and Sherren [17]). But it is impossible to say how far the characters manifested under these conditions by deep sensibility are normal, and how far they are due to incomplete regeneration.

We therefore determined in our experiment on nerve division to bring this question to a direct issue. A large area of skin was to be robbed of its sensory functions entirely, but the sensibility of the deep parts was to remain undisturbed. By this means, we hoped to have the opportunity of discovering the nature of the sensibility subserved by the afferent fibres of the nerves to the muscles and other deep structures. The result far exceeded our expectation. We found that deep sensibility is an important factor in the sum of afferent impulses which pass into the central nervous system. For the impulses conducted by the afferent fibres of these deep nerves underlie our sensations of tactile and painful presure, of the locality of deep touch, and of the position of the parts in space.

All these sensory qualities are associated with some aspect of pressure, and all are undisturbed by the denervation of the skin. They can therefore be united into one group under the name of "deep sensibility," which will form the subject of the present chapter.

The observations upon which the statements in this chapter are based were made between April 26 and July 20, 1903, when cutaneous sensation began to return to the back of the hand. During this period the sittings occupied twenty-two separate days; so that we had ample opportunity for studying the peculiar behaviour of a part where the skin had been rendered totally insensitive.

(1) Tactile Pressure.

As soon as H. regained consciousness after the operation, he was delighted to find that no part of the back of the hand was insensitive to a touch with the finger or similar hard object. The next day he was carefully tested by Mr. Sherren, who found that over the area of cutaneous insensibility on the back of the hand a pressure-touch with the rounded end of a pencil was not only appreciated every time, but was localized to within ½ in. (1·25 cm.) of the spot touched.

Nine days after the operation, Dr. Rivers summed up the results of an extended series of observations in the following words:—

"The most striking features of the examination of May 4 were that slight pressure on the abnormal area of the skin was appreciated and could be localized, whilst touches with cotton wool or deformations of the skin, caused by drawing a hair outwards, produced absolutely no sensation."

Whether a sensation was or was not elicited, when a thick camel's hair brush was applied to the dorsum of the hand, depended largely on the way in which the brush was used. If applied suddenly and vertically to the skin so as to cause a jar, a slight sensation of touch was produced; but when the pressure was made more gradually, no sensation was appreciated until distinct deformation of the brush occurred. Even in this case slight pressure only was necessary to evoke a sensation.

In the same way, stroking the part gently with a wisp of cotton wool was entirely unperceived, in spite of the thick growth of hair on the back of H.'s hand. But cotton wool, balled together into a "swab," such as is used for sponging a wound, caused a sensation if pressed upon the affected area. Slight pressure with such a ball of cotton wool might be perceived when it was put on or taken off only, and it was possible to place it on the skin with so slight a pressure that it was not appreciated at all.

The more gradually contact was established between the stimulating object and the affected part, and the smaller the pressure applied, the less likely was it that a sensation would result. All our observations showed that parts endowed with deep sensibility only are especially sensitive to jarring impact.

Not even stimulation with No. 8 of von Frey's hairs could be recognized, when applied to the affected area on the back of the hand.

When the skin was gently raised between the finger and the thumb so as to form a loose fold, it was found to be entirely insensitive, even to grave pressure.

Similarly, no sensation was experienced when considerable traction was exerted on a hair; the skin could be elevated to the maximum extent until the hair was pulled out, and no sensation was evoked. But a scarcely visible deformation of the skin by pressure was at once appreciated.

On several occasions, when the back of the hand was deeply frozen with ethyl chloride, touches were distinctly appreciated on the frozen area. On one occasion, H. stated that he could recognize no difference between the touches on the frozen portion and those on the surrounding parts. In this observation, not only was any possible sensibility of the skin excluded, but also that of the more superficial layers of the subcutaneous tissues, and it shows that they are endowed with sensibility at a considerable depth.

Several introspective observations were made on the character of the sensations of deep touch. On one occasion, H. recorded that without careful attention, no difference in quality would have been noticed between touches produced by pressure on the anæsthetic and normal areas. Pressure with the head of a pin on the normal skin produced a tactile sensation, together with sensations of slight cold and of hair-stimulation. On the affected area, the latter elements were no longer present, but the fundamental quality of the sensation seemed to remain the same, so that when the head of the pin was passed across the border separating the normal and affected areas, a considerable effort of attention was necessary to detect when the change occurred. The differences in quality were of such a kind that it is very improbable they would be noticed by any but a trained observer. On a later occasion, observations were made by stimulating the normal right hand covered with a thin rubber glove, when H. noted that the quality of the touches resembled that experienced from the abnormal area.

The most extended observations were made on the back of the affected hand, because of the rapidity with which sensation began to return to the skin of the forearm. But during the short time at our disposal, the anæsthetic parts of the forearm were found to behave exactly in the same way as the insensitive area on the dorsum of the hand.

In conclusion, there is no doubt that the back of the hand was so sensitive to contact, that most observers would have said the sensation of touch was unaffected.

(2) Roughness.

One of the most striking features of a part endowed with deep sensibility is the ease with which roughness can be appreciated.

The utility of Graham Brown's æsthesiometer depends on our power of appreciating roughness, when small cylinders are made to project for a measurable distance from a smooth metal surface. When these projections can be perceived, the sensation is one as if the part was "raked." It was found that, in this respect, the affected parts of the left hand were in no way inferior to similar parts of the right hand.

Thus on June 7 the following readings were obtained:—

	R. (sound).	L. (affected).
0·025 mm.	Not appreciated	Not appreciated
0·033 mm.	Slightly rough	More definitely rough.
0·041 mm.	Definitely rough	Definitely rough.

There was no gross difference between the two sides, but, if anything, the superiority was on the side of the affected hand. On this occasion, H. dictated the following note: "When the instrument was moved across the first interosseous space, I was more certain on the left hand than on the right that it was smooth or rough. On the sound hand I was more frequently confused by the sensations which arose from the necessary contact with hairs; no such confusing accessory sensations arose on the abnormal hand. The sensation of raking was much purer on the affected side."

If the anæsthetic skin was gently lifted into a large fold, this roughness ceased to be appreciated until the projections were extended to 0·65 mm. or 0·75 mm. Even then, the "raking" was rarely appreciated, and it was doubtful whether this sensation was not due to traction communicated to deeper structures.

Thus, the power of appreciating roughness is evidently a function of deep sensibility. Complete anaesthesia of the skin, far from diminishing this sensation, seems to make its recognition slightly more easy by removing the possibility of other disturbing sensations.

(3) Painful Pressure.

Although the skin of the affected area was totally analgesic to prick and to the painful interrupted current, excessive pressure produced a characteristic aching pain over the back of the hand from the beginning of the experiment.

The first measurements with the pressure algometer were made on June 7, and resulted as follows:—

	R.	L.
First series	4	1·5
	4·5	2·0
	4	2·0
Second series	3·5	3·5
	3·5	2·0
	4·0	2·5

Another series gave the following results, when pressure was applied in the first interosseous space:—

R.	L.
3·25	2·0
2·5	2·5
3·25	1·75
3·25	2·0

These observations showed so consistent a tendency for lower readings to appear on the affected than on the sound hand that pressure was increased, until H. said the pain was severe. This point was reached on the left (affected) side at 3·5, at 5 on the right (sound) hand.

There were local differences on both sides in the amount of pressure necessary to cause pain, but in every case the readings were less over the affected area than over similar parts of the sound hand.

Comparative readings were taken over the second metacarpal bone and over the interosseous space, with the following result:—

	R.		L.
Over the metacarpal bone	4	3	2	2
Over the muscle of the interosseous space	3	4·25	3·5	3·25

H. thought that the difference between the two hands lay not so much in the quality of the sensation as in the way it developed. On the affected side, pain emerged rather quickly as a definite aching from a dull sensation of deep pressure. On the sound side, the development was more gradual out of a mixed general sensibility. Desire to withdraw the hand was more urgent on the affected side. Moreover, H. said, "I feel more frightened at the application of pressure on the affected side."

When the algometer was pressed on a raised fold of skin against counter pressure of R.'s fingers, no pain was produced with pressures of 85. On the normal side, pain was produced with a pressure of 2.25.

Thu in conclusion we can say that it is one of the properties of deep sensibility to answer to the stimulus of excessive pressure by the production of pain. This pressure-pain is apparently wholly due to the activity of those nervous structures which are not interfered with by complete denervation of the skin.

(4) Localization.

The most surprising quality of this deep sensibility is the ease with which tactile pressure is localized. Three methods were employed for testing the power of localization. First, H. kept his eyes closed, but tried to point to the spot touched with his right hand; or he was allowed to open his eyes and point, without contact with the skin, to the place he supposed had been touched. Lastly, R. touched the affected area at a spot he had marked on a life-sized photograph of the left hand, whilst H. attempted to mark the spot on a similar photograph. This is the method of Victor Henri [19], and in this case it gave surprisingly good results.

A fortnight after the operation, on May 9, it was found that of twenty-nine touches within the affected area, seventeen were quickly appreciated and accurately localized, six were not localized correctly, and six were not appreciated at all. It must be remembered, that at this stage the skin over the affected area was swollen, which somewhat hindered these experiments. The passing away of the swelling rendered the later experiments even more striking.

On May 17 a series of twenty-four observations was recorded by Henri's method on life-sized photographs. The results were remarkable, and it could not be said that there was any difference between the two hands in the quickness and accuracy with which pressure, touches were localized.

R. chose nine spots in various parts of the affected area unknown to H.; these are marked in black on the annexed figures (figs. 15 and 16). The following table gives the places stimulated in order and the position of the spots marked by H. on his photograph:—

(2) Localized exactly.

(3) Localized 1·3 cm. from the spot touched.

(4) Localized exactly.

(8) Lay over the interphalangeal joint of the thumb, and was localized near the metacarpo-phalangeal joint at a distance of 2·5 cm.

(1) Localized exactly.

(9) Over metacarpal of thumb—localized at a spot 2·5 cm. distant in interosseous space.

(6) Localized 0·5 cm. from spot touched.

(5) Localized 0·75 cm. from the spot touched.

(7) Localized 1·0 cm. on the proximal side of the point touched.

(2) Localized exactly.

(4) Localized exactly, so much so that the mark of the previous record was identical with that of this stimulation.

(7) Localized 1·0 cm. from point touched over the same spot as before.

(6) Localized exactly.

(8) Localized exactly.

(9) Localized 3 cm. distal to the spot stimulated.

(7) Localized exactly.

(3) Localized exactly.

(6) Localized exactly.

(7) Localized exactly.

(9) Localized 2 cm. distal to the point stimulated.

(3) Localized exactly.

(8) Localized exactly.

(2) Localized exactly.

(6) Localized exactly.

An image should appear at this position in the text.

Fig. 15

Reduced to two-thirds the natural size (May 17, 1903).

Certain spots were marked on a life-sized photograph of H.'s hand. These are shown by black numbers within a circle of 1 cm. in diameter.

H. was given a similar photograph and marked upon it in each case the spot he thought R. had touched.

The photograph showing the spots stimulated and that showing H.'s localization have been combined; the marks made by H. are printed in red. Thus, for instance, a red 3 shows the spot marked by H. as the locality of a stimulus applied by R. to the area marked with a black 3.

The order of stimulation is given in the text.

An image should appear at this position in the text.

Fig. 16

In order to test the localization over the spots 8, 7, 6, 9 and 3 two photographs of the lateral aspect of the hand were used exactly as described under fig. 15. These have been combined in the same way and the marks made by H. have been printed in red.

Point 2 was touched three times and in every case was localized exactly.

Point 3 was localized twice exactly and once 1·3 cm. from the spot touched.

Point 4 was localized twice exactly.

Point 6 was twice localized exactly and twice within 0·75 cm. of the spot touched.

Point 7 was twice localized exactly and twice 1·0 cm. from spot touched. The two erroneous localizations fell over the same point.

Point 8 was twice localized exactly. Once it was localized over the proximal joint at a distance of 2·5 cm.

Point 9 showed the worst localization of any of the spots chosen, and was always localized distal to the point of stimulation; twice 3 cm., and once 2 cm.

Thus, all our experiments showed that the localization of a touch sufficiently heavy to cause a sensation was remarkably accurate. This power of localization remained after freezing with ethyl chloride, though, owing to the haste with which such observations had to be made, it was somewhat less accurate than at other times.

(5) Spacial Discrimination (Compasses).

In spite of the remarkable power of localization, H. was entirely unable to discriminate one from two points of the compasses, even when separated for the widest distance permitted by the size of the affected area on the hand, 6 cm. in a direction longitudinal to the axis of the limb. And yet, over a similar part of the normal hand, a perfect record was obtained at 2 cm.^[1]

But, as soon as the second point was placed upon the skin a fraction of a second later than the first, H. at once recognized that he was being touched in two places.

When the compasses were 3 cm. apart, he called every simultaneous contact "one," whilst four out of five stimulations with two points successively were recognized and the fifth was said to be doubtful:—

Even at a distance of 1·5 cm. H. was surprisingly often right in his answers provided stimulation was successive:—

On the sound side the formula was as follows:—

And in every case where a right answer was given, H. recognized whether the two points were applied simultaneously or successively.

Thus it is evident that the presence of deep sensibility alone does not make it possible to discriminate two points applied simultaneously.

(6) Appreciation of Size and Shape.

All appreciation of size was lost over the affected area endowed with deep sensibility only. Even the flat and the edge of a knife could not be distinguished from one another. H. seemed to have no power of telling the relative size of a series of wax figures, although he at once recognized the relative pressure with which they were applied.

A small square of 1 cm. was placed on the skin with considerable pressure and compared with another figure 4 cm. in diameter applied with little pressure. H. made no statement with regard to the relative size of the objects, but said the first gave a sense of greater pressure. This was repeated many times on different occasions with the same result.

All power of telling the head from the point of a pin was entirely absent over the affected parts.

Unfortunately, the size of the area on the hand did not permit of the complete application of tests for shape. It was found that even a circle, a square or a triangle, cut out of wax so that all lay entirely within a 4 cm. square, could not be distinguished with certainty on the dorsal surface of the sound hand. But, although the answers were wrong as regards the shape, H. had a definite sensation of pressure on a circumscribed surface, a surface with borders and angles. On the affected hand, the sensation was one of pure pressure accompanied by no idea that the object by which the pressure was produced had any shape. Thus, on June 22, it was noted that on the back of the left hand there was a complete absence of any element of shape in the sensations. Pressure was experienced, and this was well localized, but there was nothing to indicate that the body producing the pressure had any shape. But on the sound side there was a distinct impression of form, chiefly of angles here and there, though the total shape could not be perceived correctly.

When a very large surface was applied, H. thought it seemed to him large, because he had a visual picture of his hand on which he had certain points of reference, such as the first and second metacarpal bones with their tendons. He imagined the object was large, because he perceived a sensation from both these widely separated places. But this failed entirely if both spots could be touched strictly simultaneously when the large object was applied to the skin.

(7) Perception of Movement on the Skin.

In some of the observations in which the skin was stimulated successively with compass-points, the sensation produced was not so much one of "twoness" as of rocking or pushing on the skin. This led us to test whether the affected area was especially sensitive both to progressive movement over the skin and to rotatory movement of a round object in which the stimulated area of the skin remained the same.

Slight movements were readily appreciated on the affected side, but we could not detect any definite difference in sensitiveness between the two hands.

(8) Recognition of Muscular Movement.

Head and Sherren ([17] p. 214) were able to show that perfect recognition of passive movement of the joints was possible when the nerves to deep parts alone were intact. In the case of H. we had no means of attacking the problem, for no part of any finger was totally insensitive to cutaneous stimulation.

But we were able to show that the interrupted current could produce sensation by contracting the muscles only. Even the slightest contraction of the abductor indicis or the adductor pollicis produced a distinct sensation of movement, localized in the muscle. No pain was evoked, unless the muscle was thrown into cramp.

(9) Temperature.

The existence of deep sensibility conveys no capacity for appreciating stimulation with any degree of temperature. Ice and water at 60° C. were equally incapable of evoking a response over the affected area of the hand. The parts could be frozen stiffly with ethyl chloride, and H. remained unconscious of any stimulation, provided the normal skin was carefully protected with a thick layer of impervious material.

This freezing produced a numb aching, in no way allied to a thermal sensation, but resembling the "numbness" produced by extended exposure of the hands to severe external cold.

In conclusion, we have shown that the peculiar aptitude possessed by a part innervated solely by the afferent fibres of a muscular nerve is the appreciation of all stimuli which produce deformation of structure. Pressure or jarring contact are quickly appreciated and localized with remarkable accuracy. "Roughness" is as well recognized on the affected as on the sound hand.

Two points can be discriminated if applied successively, but not when contact is made strictly simultaneously.

Although pressure is well localized, all sense of relative size is lost over the affected parts.

Excess of pressure produces an aching pain; and the cramp, caused by repeated electrical stimulation of the muscles, is at once appreciated.

Pressure, which ordinarily causes a sensation of touch or of pain, produces no effect upon consciousness when applied to a fold of skin elevated into a ridge, thus proving that the sensations which are present are not due to any end-organs remaining in the skin.

The presence of deep sensibility conveys no power of appreciating any temperature stimulus.

1. Occasionally, when the compasses were applied over the anesthetic skin of the forearm with the points at distances exceeding 10 cm., H. recognized them as two. But he was clear that this depended on the localization of one point at one place and the other in widely distant part of the limb. He had no sense of inevitable "twoness," as when the two points were separated to a distance above the threshold on the normal skin. The process was one of judgment, in that he knew he was being touched near the wrist and also somewhere up the forearm.