The Sensational Contributions of Erik Moberg by Dellon A Lee
The Sensational Contributions of Erik Moberg by Dellon A Lee
A. LEE DELLON
From the Department of Plastic Surgery, Johns Hopkins University, Baltimore, Maryland, U.S.A.
Erik Moberg is the father of functional sensory testing. During the past three decades, his research
into quantitative testing of hand sensibility has provided the insight to bring us from classic academic
tests (permitting localisation of lesions within the central nervous system) to clinical capability of
restoring sensation to the hand. He introduced the Ntiydrin test to document objectively innervation.
He defined hand function as precision-sensory and gross-sensory grips. He correlated Weber two-
point discrimination with hand function. He introduced the pick-up test to document hand function.
He coined the term “tactile gnosis”. He hypothesised that proprioception is principally due to skin,
not joint, tierents. He classified the tetraplegic hand according to its combined sensory and motor
capacity. He set the standard foF.sensory recovery after primary nerve repair, relating recovered
two-point discrimination to age (Onne’s line) and he inspired the present generation of researchers
to quantify their own studies of sensation.
Journal of Hand Surgery (British Volume, 1990) 1.5B: 14-24
“It must be emphasized that sensibility is, in my stage for the foreseeable future in terms of evaluation of
opinion and according to my experience, the basis sensibility and rehabilitation of sensory function.
for reconstructive work , . . for reconstructive Moberg, as a young orthopedic surgeon working on
surgery, “feeling” is a totally useless term, as it the Hand Service at Sahlgren Hospital in Gijteborg, was
covers far too much and distinguishes hardly required to carry out yearly re-examinations on work-
anything . . . for examination of useful sensibility men’s compensation patients. Thus, he had an opportu-
in reconstructive hand surgery, of all the tests nity to attempt to evaluate sensibility and correlate the
evaluated by the author, the only one which was results of his testing with the patient’s ability to use their
found to be significant is the two-point discrimina- hands. It was clear to Moberg that the academic tests
tion test now performed with a paperclip. All other developed by neurologists, such as testing for the
tests of sensory function, in my opinion, should in perception of sharp or dull, or of pain with a pin or of
this work be abandoned, including cotton wool and movement with a cotton wisp, were inadequate to
paper strip, pinprick, ordinary tuning fork, the determine whether a person could use their hand or not.
difference between sharp and blunt, figure writing, He thus developed (Moberg 1958) his own functional
the wrinkling skin test and the two-point discrimi- test, the “picking-up test” (Fig. 1). The blindfolded
nation test performed with sharp pointed compass. subject would be asked to pick up common objects and
They are not only useless, they are even misleading.” put them into a container. He also could be asked to
Erik Moberg. identify these objects and could be timed while doing so.
The results of this picking-up test could then be compared
At the Seventeenth Annual Meeting of The American with the academic tests and with the Weber two-point
Society for Surgery of the Hand, held in San Francisco, discrimination test (Weber, 1835). While the results of
on May 14, 1962, Erik Moberg was honoured with the this study would not be reported for four more years
privilege of presenting the first Memorial Lecture for the (Moberg, 1962), this 1958 paper clearly described the
man who “wrote the book” in our field, Sterling Bunnell. first functional test for the hand, thereby setting the stage
Moberg recalled having had the opportunity to hear for what today represents a host of tests designed to
Bunnell teach shortly after World War II. He was evaluate hand function (Baxter and Ballard, 1984).
impressed with Bunnell’s “priority for restoration of Moberg realised that most tests of sensory function
sensory function”, a principle which Bunnell stressed in were subjective, in that the patient was asked how he
his book and in teaching his pupils. Moberg said in that perceived something : none of the tests was truly objective
lecture (Moberg, 1964) that, since hearing Bunnell speak, i.e., without the ability for the patient to influence the
“I have never been able to leave the question of sensibility result. Accordingly, he developed the first truly objective
in hand function”. Moberg had been impressed with test of sensory function (Moberg, 1958), utilising tests
Bunnell’s powers of observation and ability to coin that had been developed for finger-printing criminals. In
concise expressions, such as “no-man’s land”, abilities one technique, he would take paper on which had been
which .were keenly possessed by Moberg himself. By the sublimated iodine crystals staining the paper yellow, and
time of the delivery of this First Annual Sterling Bunnell then make a fingerprint upon the paper. In the other
Memorial Lecture, Moberg already had contributed his technique, the fingerprint was made first, placing the
own fundamental observations and his own newly-coined amino-acids from the sweat onto the paper, which was
expressions (Moberg, 1958 and 1962) that were to set the subsequently sprayed with a solution of Ninhydrin.
Fig. i The picking-up test as described by Moberg in 1958. This test employed constant touch and required a precision sensory grip
Punctate dots appeared at each sweat duct opening. The Neurologists had previously used two-point discrimina-
Ninhydrin method left a print that could be preserved. tion as a measure of a parietal lobe function termed
The starch iodine technique developed quickly but was “stereognosis”. Moberg attributes the term “tactile
not easily preserved. Moberg went on to make the critical gnosis” to Broman in 1945, suggesting that it be used for
observation that the tests of sudomotor function clearly “knowing touch” or seeing with the fingertip (Fig. 2).
demonstrated whether nerve function was present or not. Tactile gnosis, therefore, refers specifically to the sensi-
However, the fact that nerve function was present in no bility present in the fingertip being sufficient to permit
way correlated with the final functional ability of the the perception of neural impulses as a meaningful
hand. Thus, the Ninhydrin and starch iodine tests were conscious perception, i.e., functional sensation. In his
an objective method for evaluating malingerers or 1962 paper, in which correlations were made, Moberg
children, comatose or uncooperative patients, but the concluded that only the classic Weber two-point discrim-
result was not a predictor of hand function. ination test, which he had performed utilising a compass
In this first critical paper in 1958, Moberg introduced with blunted tips (so it did not produce pain), correlated
the term “tactile gnosis” to the surgical community. with the results of the picking-up test. Therefore, only
the Weber two-point test was a functional test and of use
to the hand surgeon whereas the other tests were more of
a value as academic tests, as developed by the neurologists
to localise lesions in the central nervous system.
“When eyesight is to be tested, it is considered
necessary to find out what the eye can see. When
we wish to determine improvement or impairment
of function of the ear, we try to find out what the
ear can hear (Fig. 3). Why not test the sensory
function of the hand? Why should the mere
perception of touch (with cotton wisps) or pain
(with a pin) by the hand be accepted as a sign of
normal sensation, when perception of light never
was identified with a normal capacity to see?”
Moberg 1964
Moberg set the stage for the later developments of
sensory rehabilitation. In discussing the results or nerve
repair, he stated that “As a matter of fact, it is astonishing
that improvement can be obtained at all. Nature must
provide a helping hand” (Moberg, 1964). He observed
that sensation continued to improve in its level of
Fig. 2 Moberg coined the term “tactile gnosis”. recovery for five years after a median nerve repair at the
nerve repairs. This work (&ne, 1962) remains a classic. AGE (years)
It demonstrates that the degree of sensation recovered in Fig. 4 Moberg suggested that the best way to report the results of
millimetres of two-point discrimination is equal to the nerve reconstruction would be to relate the patients’ age with
his two-point discrimination, The “ideal” result was that
patient’s age in years at the time of the nerve repair. The determined by ijnne (1962) in evaluating Moberg’s five-year
patients had been evaluated five years after the repair. results following a clean division and primary repair of the
Moberg was to suggest subsequently (1975) that, since it nerve (Gnne’s line).
RIGHT
Medical Society and subsequently published in the Johns
Hopkins Medical Journal (Dellon, Curtis and Edgerton,
1972). The functional sensibility of the hand is mediated
through the large myelinated (group A beta) fibres. Tests
for hot and cold, sudomotor function and pain are
mediated through the thinly myelinated (group A delta)
and non-myelinated (group C) fibres. Therefore, tests for
hot, cold, pain and sudomotor function cannot predict
the outcome for tactile gnosis. Among the group A beta
fibres, some are quickly-adapting and some slowly-
adapting. Precision grip, gross grip and the pick-up test
require the patient to know that an object is held in
constant touch between the fingers and to know how
hard to press to prevent the object from falling out of the
hand. The Weber two-point discrimination test measures
the innervation density of these slowly-adapting group A
beta fibres and therefore would be the test to predict the
Fig. 6 Up to 67 discrete areas have been suggested as the appropriate findings Moberg observed.
way in which to measure both cutaneous pressure threshold Moberg did not attempt to measure the cutaneous
and two-point discrimination for detailed sensibility evaluation pressure thresholds by means of Semmes-Weinstein
of the hand.
monofilaments, as these were not produced until 1962. It
may be speculated that Moberg would have found a
teaching have come Judy Bell and Ann Callahan, under relationship between the speed with which the patient
whose continuing direction cutaneous pressure threshold could carry out the pick-up test and a correlation with
measurements have reached their acme (Bell-Krotoski precision and gross sensory grip with the von Frey type
and Tomancik, 1987). testing apparatus, had it been available to him (Dellon
and Kallman, 1983). Recognising that the group A beta
fibres also contain a quickly-adapting sub-set, the
Neurophysiological basis for Moberg’s clinical observa- possibility of testing moving touch in addition to constant
tions touch and the possibility of using tuning forks of varying
Erik Moberg’s influence was extended to Baltimore frequencies to evaluate the sub-set of the quickly-
through his association with Raymond M. Curtis who adapting fibres was realised. These realisations culmi-
was a direct disciple of Sterling Bunnell and began the nated in the identification of the sequence of recovery of
Hand Surgery School in Baltimore. As a medical student touch sub-modalities following nerve regeneration : the
at Johns Hopkins, I encountered Dr Curtis in the Hand first to recover (after pain and sudomotor function and
Surgery Conference on the Plastic Surgery Service at the perception of cold and heat) is perception of the 30 cycle
end of my second year of medical school. In the summer per second stimulus, then moving touch, then constant
of 1968, between my second and third year of medical touch and finally 256 cycle per second vibratory stimulus
school, I received permission to watch Dr Curtis (Dellon, Curtis and Edgerton, 1972). The tuning forks
operating. He inspired me that summer to spend the used are shown in Figure 7.
major effort of my research on peripheral nerves and Erik Moberg visited Raymond Curtis in Baltimore
upper extremity reconstruction. Having been exposed to during the academic year 1969-70 which provided me
the neurophysiological investigations of Vernon B. with my first opportunity to meet Professor Moberg.
Mountcastle during my physiology course at Johns Moberg listened patiently while the theories of the above
Hopkins, it was natural to attempt to provide a paragraph and their applications to sensory rehabilitation
neurophysiologic basis for the clinical evaluation of the were described. At this time, sensory re-education based
hand that I had seen being carried out by Dr Curtis, who on the institution of specific sensory exercises at the
turned me to the 1958 and 1962 writings of Erik Moberg. specific time in the recovery process, as determined by
The possibility of attempting to provide the neurophy- the evaluation of sensibility, was being developed.
siological basis for Moberg’s observation that Weber Moberg was extremely encouraging of this early work
two-point discrimination could predict the outcome of and his enthusiasm further strengthened Curtis’ support
whether a patient would have precision or gross sensory for this early work. Subsequently, the first efforts in
grip, the outcome of the pick-up test and the explanation sensory re-education were presented to the American
of why the classic academic tests could not predict such Society for Surgery of the Hand at their 1971 Meeting
function proved to be a challenge. The hypothesis was (Dellon, Curtis and Edgerton, 1974). The discusser of
presented on February 3, 1969 to the Johns Hopkins that paper was Svante Edshage, Moberg’s pupil and
other . . . In important parts of basic neuroscience The concept that in nerve compression there is a
and clinical nerve work the situation has been gradation in which first there are threshold changes and
similar . . . The young author of this book is the then innervation density changes has been documented
first one to connect these two antipodes, each so experimentally in subhuman primates (Dellon, 1983) as
important to the other . . . Dr Dellon’s enormous well as in hands of experimental subjects (Szabo et al.,
enterprise, to travel through and scrutinise modern 1984) and in the legs of surgical house officers (Phillips et
physiology and other basic sciences and to summar- al., 1987). The first changes in acute or chronic nerve
ise and combine these with modern hand surgery compression are threshold changes which are clinically
reminds one of the ancient explorer Marco Polo. . . manifested by numbness and tingling and can be most
this book is unique in the flood of hand surgery easily tested by alterations in perception of a 256 cycle
literature of today. No doubt it will give rise to per second tuning fork compared with an opposite
conflicting opinions and controversy, which is the extremity, but may be documented by any of the
basis of all progress.” techniques for measuring threshold changes. Then there
are electrical changes which can be measured. It is not
until nerve fibres are lost, i.e., the electrical testing
becomes unresponsive, that two-point discrimination is
Threshold versus innervation density
altered.
The apparent conflict in the world of sensibility evalua- Following nerve repair and nerve regeneration, the
tion lies between those who champion the use of threshold first physiological parameters to recover are threshold, as
measurements (such as Semmes-Weinstein nylon mono- there are very few nerve fibres at the extremity so two-
filaments) to measure cutaneous pressure threshold and point discrimination cannot be tested. Thus, it is most
those who champion measurements of innervation appropriate early in the course of nerve regeneration to
density (i.e. two-point discrimination). Understanding test for threshold changes, not innervation density.
the physiological response to nerve injury permits the Considering the sequence of recovery following nerve
rational choice of the clinical test of sensibility and injury (Dellon, Curtis and Edgerton, 1972), first a 30
resolves this conflict. The distinction is generally appre- cycle per second tuning fork may be utilised and then a
ciated for the motor system : the early clinical manifesta- 256 cycle per second tuning fork. Alternatively, nylon
tion is muscle weakness but once motor nerve fibres monofilament determinations may be made. Once the
degenerate, there is also muscle wasting or atrophy. The perception of the 256 cycle per second vibration has
analogy in the sensory system is that the first changes to reached the fingertips, enough nerve fibres will have
occur are threshold changes, such as differences in the recovered to allow one to begin measuring two-point
cutaneous pressure threshold or changes for the slowly- discrimination. At this time, continued orderly progres-
adapting fibre receptor system or changes in the cutaneous sion towards a plateau at some level of threshold may be
vibratory threshold for the quickly-adapting fibre recep- expected and threshold determinations need not be
tor system. Thus, in compression of the median nerve at measured theafter. Two-point discrimination, both static
the wrist, the patient will have an altered perception of a and moving, may be tested with the expectation that
vibratory stimulus applied to the index finger when these will continue to improve for a period of years at a
compared with the little finger of the same hand (Dellon, speed which will be determined by the amount of sensory
1980b). Semmes-Weinstein testing would show two re-education given in the post-operative period.
different thresholds of the index versus that in the little
finger. Vibratory thresholds could be quantitated with a
Current evaluation of sensibility
Vibrometer (Dellon, 1983). As there exists a whole
battery of nylon monofilaments, one can envision testing Erik Moberg’s influence continues to inspire new
the whole spectrum of frequencies and determining their attempts to quantify sensibility and thus improve the
stimulus intensity (i.e., threshold) at each frequency to capacity of the reconstructive surgeon to restore sensation
determine an audiogram for the finger. This was first by enabling him to compare different methods accurately.
proposed by McQuillan in 1970 and G&an Lundborg, a Microvascular surgery gave us the ability to replant digits
student with Moberg in Goteborg, has developed such and transplant toes. After the initial excitement over the
an instrument (Lundborg et al., 1986). vascular triumph of these techniques, the emphasis was
In the sensory system, once nerve fibres have degener- placed on rehabilitation. The results of sensibility testing
ated, there is a decrease in innervation density and this and sensory re-education in this population ,of patients
is measured by alterations in two-point discrimination. utilising the sensory testing techniques described above
When the static 2 P.D. becomes abnormal, slowly- has been reported (Dellon, 1986). Various sites for
adapting fibre receptors have been lost. When the moving innervated free-tissue transfers exist and their true
2 P.D. becomes abnormal, the quickly-adapting fibres potential for sensory function is unknown. Discrimina-
have been lost. tive capacity, even in these normal tissues, was improved
Conclusion
the force at which the two prongs are applied. Bell,
working with Frank Kanatani, developed a prototype The sensational contributions of Erik Moberg have come
for this instrument (Fig. 12) which allows adjustment of full circle in that one of Moberg’s earliest and continuing
the force applied to the two wire prongs of their concerns was how hard to press the paperclip onto the
instrument by altering the length of the wire; the force is finger. His first efforts indicated that the prong should be
specified by the wire bending at the time it is applied. applied no firmer than is necessary to blanch the skin.
The space between the two wire prongs would be varied
by having a series of the test instruments. Most recently, tPost Office Box 26335, Minneapolis, Minnesota 55426, U.S.A.
Fig. 13 The force-defined two-point discriminator prototype. (a): A strain gauge at the base of each of the two prongs permits a continuous read-
out of the force required to deliver the stimulus at which the patient can determine whether one or two points are on the skin. The distance
between the two prongs is adjusted by the micrometer. (b): One of the two prongs may be “disengaged” to permit the use of the single
prong as a cutaneous pressure threshold measurement as well. The instrument can test both moving and static 2 P.D. and the final force at
which the determination was made. (By permission of N.K. Biotechnical Engineering Company)
His concern was that pressing onto the surface of the DELLON, A. L., SCHNEIDER, R. J. and BURKE, R. (1983). Effect of Acute
Compartmental Pressure Change on Response to Vibratory Stimuli in
skin would deform the skin and create an error, in that Primates. Plastic and Reconstructive Surgery, 72: 2: 208&2!6.
you would be measuring not what occurred just beneath FESS, E. E. Documentation: Essential Elements of an Upper Extremity
the prong but over a greater area. This problem is solved Assessment Battery. In: Hunter, J. M., Schneider, L. H., Mackin, E. J. and
Callahan, A. (Eds.), Rehabilitation of the Hand, (2nd edn.), St. Louis, C. V.
now by being able to specify the force at which the 2 Mosby, 1984: 49978.
P.D. measurement is made. After all, Moberg’s chief LEVIN, S., PEARSALL, G. and RUDERMAN, R. J. (1978). Von Frey’smethod
concern was what the finger would do and it is therefore of measuring pressure sensitivity in the hand: An engineering analysis of the
Weinstein-Semmes pressure aesthesiometer. Journal of Hand Surgery, 3: 3:
more critical to know what is happening over the surface 211-216.
of the phalanx than at a given spot. Moberg echoed LUNDBORG, G., LIE-STENSTRijM, A.-K., SOLLERMAN, C., STROM-
BERG, T. and PYYKKij, I. (1986). Digital vibrogram: A new diagnostic
Bunnell in saying that “Without sensation, the hand is tool for sensory testing in compression neuropathy, Journal of Hand Surgery,
blind”. Today, with appropriate evaluation of sensibility, 11A: 5: 693-699.
reconstructive surgery to restore sensation and sensory MACKINNON, S. E. and DELLON, A. L. (1985). Two-Point discrimination
tester. Journal of Hand Surgery, 10A: 6(l): 906-907.
re-education, we are confident that the future will permit MACKINNON, S. E. and DELLON, A. L. Surgery of the Peripheral Nerve,
us to say “even the blind hand can see”. York, Thieme, 1988.
McQUILLAN, W. (1970). Sensory recovery after nerve repair. The Hand, 2: I :
7-9.
MOBERG, E. (1955). Discussion of Brooks, D: “The place of nerve-grafting in
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0 1990 The British Society for Surgery of the Hand
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