Origins of the Sensory Examination
in Neurology
Cassiopeia Freeman1 and Michael S. Okun, M.D.1
ABSTRACT
Formal testing of sensation as part of the neurological examination followed the
improvements in examination techniques as well as advances in neuroscience. By the
1890s, the observation that temperature sense was frequently impaired at the same time
that pain was appreciated led to the supposition that the two paths traveled closely.
Through the works of Brown-Séquard and Edinger the existence of a crossed afferent
tract was verified. The distinction between two sensory pathways was clear by 1898, when
van Gehuchten reported a case of syringomyelia and suggested that the pain and temperature fibers were carried anterolaterally and the position sense fibers carried posteriorly in
the spinal cord. Many authors describing patients with tabes dorsalis suspected the posterior columns of the spinal cord played a key role in position sense. It is difficult to determine in the 19th century who first employed the use of movements of joints as a test for
proprioceptive function; however, Bell in 1826 recognized what he termed a sixth sense,
which later was characterized as proprioceptive function. Goldscheider went on to report
the degrees of movement that were considered normal for each joint. Although vibratory
sense had been described by Cardano and Ingrassia in the 16th century and tests had
been developed by Rinne and Rumpf by the 19th century, it was not until 1903 that Rydel
and Seiffer found that vibratory sense and proprioceptive sense were closely related and
that both senses were carried in the posterior columns of the spinal cord. By 1955, the
sensory examination included tests for light-touch, superficial pain, temperature, position
sense, vibration, muscle (deep pain), and two-point discrimination. Tests for these sensibilities still remain in use. We will review the origins of the understanding of sensation,
which ultimately led to the development of the sensory examination. We will highlight
individuals who made important discoveries and observations, as well as review the history of each of the elements of the sensory examination.
KEYWORDS: History, sensory, examination, neurological, tuning fork, pinprick,
proprioception, two-point
Objectives: Upon completion of this article the reader will be able to cite the seminal observations in our understanding of the sensory system and its application in the neurological examination and neurological diagnosis.
Accreditation: The Indiana University School of Medicine is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians.
Credit: The Indiana University School of Medicine designates this educational activity for a maximum of 1.0 hours in category one
credit toward the AMA Physicians Recognition Award. Each physician should claim only those hours of credit that he/she actually
spent in the educational activity.
Disclosure: Statements have been obtained regarding the authors’ relationships with financial supporters of this activity. There is no
apparent conflict of interest related to the context of participation of the authors of this article.
The Neurological Examination (with an Emphasis on Its Historical Underpinnings); Co-Editors in Chief, Robert M. Pascuzzi, M.D., Karen L.
Roos, M.D.; Guest Editor, Elan D. Louis, M.D., M.S. Seminars in Neurology, Volume 22, Number 4, 2002. Address for correspondence and reprint
requests: Michael S. Okun, M.D., Departments of Neurology and History, University of Florida, McKnight Brain Institute, P.O. Box 100236,
Gainesville, FL 32610. 1Departments of Neurology and History, University of Florida, Gainesville, Florida. Copyright © 2002 by Thieme Medical
Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662. 0271-8235,p;2002,22,04,399,408,ftx,en;sin00220x.
399
400
SEMINARS IN NEUROLOGY/VOLUME 22, NUMBER 4 2002
Figure 1 Wood cut from Rene Descartes (1596 to 1650) displaying reflex action external heat.
A
lthough sensory responses to external stimuli
have been appreciated for centuries (Fig. 1), the development of a related neurological examination did not
come until the late 19th century. The examination of sensation is an important part of the complete neurological
evaluation.1 The practitioner can, by utilizing an understanding of neuroscience, use normal and abnormal findings to localize the origin of a sensory disturbance. The
sensory system consists of nerves that traverse either the
spinothalamic (pain and temperature) or dorsal column
(position and vibration) pathways. The afferent fibers in
these systems relay information from the skin, subcutaneous tissue, muscles, tendons, periosteum, and visceral
organs to discrete areas of the thalamus, and finally to
the cerebral cortex.1 Disruptions in these systems provide the bedside examiner an opportunity to localize an
abnormality that may consist of a change, impairment,
or absence of a sensory perception. This chapter is comprised of three parts. First, we will review the origins of
the understanding of sensation, which ultimately led to
the development of the sensory examination. Second, we
will highlight those individuals who made important
discoveries and observations. Finally, we will review the
history of each of the elements of the sensory examination.
ORIGINS OF THE UNDERSTANDING
OF SENSATION
In 1838 Johannes Mueller (1808 to 1858) formulated
the ideas of “specific energy” and “specific irritability.”
Mueller pointed out that the same stimulus could produce
different sensations if it was applied to nerves supplying
different sensory modalities.2 This discovery later led to
Max von Frey’s (1852 to 1932) suggestion in 1894 that
there was specificity of the length of a sensory neuron
with respect to a given sensation.3,4 In 1920 Sir Henry
Head suggested that there were two specialized types of
cutaneous nerves, and this observation served as the basis
for his “specific fiber theory.”5 Although there were many
different classifications of sensation and as such many
classification systems, Head’s definitions were crucial to
our understanding of sensation. He defined the two basic
subtypes of sensation, addressing the important distinction between epicritic and protopathic sensibility.5 Head
described epicritic sensibility as the ability to make fine
discrimination of touch and temperature sensations, as
well as the ability to localize and discriminate sensation.
He went on to contrast this with the description of a very
different type of sensation. He characterized protopathic
sensation as changes in temperature and pressure without the ability to localize an abnormality.5 Additional
classifications of sensation were also suggested including
exteroceptive, proprioceptive, and interoceptive sensation, which were largely based on the end organs and the
stimuli mediated.6,7
Formal testing of sensation as part of the neurological examination followed the improvements in examination techniques as well as advances in neuroscience.8 By the 1890s, the observation that temperature
sense was frequently impaired at the same time that
pain was appreciated led to the supposition that the two
paths traveled closely.9–11 Through the works of BrownSéquard12 and Edinger13,14 the existence of a crossed afferent tract was verified. The distinction between two
sensory pathways was clear by 1898, when van Gehuchten
reported a case of syringomyelia and suggested that the
pain and temperature fibers were carried anterolaterally
and the position sense fibers posteriorly in the spinal
cord.15 Many authors describing patients with tabes
dorsalis suspected the posterior columns of the spinal
cord as playing a key role in position sense.9,10,16–18 It is
difficult determine in the 19th century who first employed the use of movements of joints as a test for proprioceptive function. However, in 1826 Bell recognized
what he termed a sixth sense,19 which later was characterized as proprioceptive function. Goldscheider went
on to report the degrees of movement that were considered normal for each joint.20,21 Vibratory sense was described by Cardano22 and Ingrassia23 in the 16th century, and tests were developed by Rinne24 and Rumpf25
by the 19th century, but it was not until 1903 that Rydel
and Seiffer26 found that vibratory sense and proprioceptive sense were closely related and that both senses were
carried in the posterior columns of the spinal cord. By
1955, the sensory examination included tests for lighttouch, superficial pain, temperature, position sense, vibration, muscle (deep pain), and two-point discrimination.1 Tests for these sensibilities still remain in use.
PEOPLE INTEGRAL IN
UNDERSTANDING SENSATION
AND THE SENSORY EXAMINATION
Various investigators were instrumental to the development of the sensory examination (Fig. 2). Here we will
highlight those individuals who made important discoveries and observations.
ORIGINS OF THE SENSORY EXAMINATION/FREEMAN, OKUN
Moritz von Romberg (1795 to 1873)
Romberg’s major contribution to the understanding of
sensation was his description of a sign that indicated dysfunction of the posterior columns of the spinal cord. During the period from 1840 to 1846, while he was director
of the University Hospital in Berlin, he wrote the textbook Lehrbuch der Nervenkrankheiten des Menschen, A
Manual of the Nervous Diseases of Man.17 It was one of
the first systematic textbooks in neurology that compiled knowledge on the physiology of the nervous system and provided precise descriptions addressing the
pathogenesis of disease. His work allowed for more directed medical treatments. Romberg described a neurological examination sign for tabes dorsalis. The Romberg
sign, as it is known today, is an indication of posterior
column dysfunction. He described the sign in patients
with tabes dorsalis (syphilis) who could not maintain
balance when standing with their eyes closed and feet
together. He noted that if the patient swayed or lost balance there was dysfunction in the posterior columns.17
Romberg, however, was not the only investigator to take
note of this important examination finding. Marshall
Hall (1790 to 1857) in his Lectures on the Nervous System
and its Diseases, described the loss of postural control in
darkness in a patient with proprioceptive difficulties.27
Additionally, in 1840 Bernardus Brach noted that patients with proprioceptive deficits were not weak even
though they could not stand or walk in the dark.28 Lanska and Goetz have noted that as Romberg’s sign became increasingly used its significance was clarified, and
patients with other diseases involving the cerebellar, ves-
tibular, pyramidal, and muscular systems could be separated from those with posterior column dysfunction.
Hence, the sign became linked to all causes of proprioceptive deficits.29
Charles-Edouard Brown-Séquard (1817 to 1894)
Charles-Edouard Brown-Séquard, the prominent British
neurologist, was the first to describe a sensory syndrome
that resulted from hemisection of the spinal cord. The
syndrome was thought to have been brought to his attention by observations of injuries of the Parisian Mafioso.
These gang thugs inflicted brutal trauma on their enemies by using stilettos that could penetrate the spinal
canal.30 Brown-Séquard observed an important sensory
phenomenon that resulted from these and other injuries,
especially when there was hemisection of the spinal cord.
What he had found was a dissociation of sensation.
Their sensory examination included a decrement in pain
and temperature sensation contralateral to the lesion and
a loss of position and vibratory sense ipsilateral to the lesion.12 Brown-Séquard additionally described associated
motor paralysis, vasomotor paralysis, disturbances of
deep sensibility, hyperesthesia of tactile impressions, and
disturbance of pain and thermal impression. He observed
vasomotor paralysis and described a reddening of the
skin with first a coincident warmth and then an intervening cold cyanosis. He noted that even after motility
returned in these patients, deep sensibility problems were
obvious when proprioception was disturbed and ataxia
was present.12
Figure 2 Top (from left to right): Romberg, Brown-Séquard, Charcot, Dejerine, Sherrington; bottom (from left to right): Head, Foerester, Gasser, Erlanger, von Frey. (Images provided courtesy of the National Library of Medicine.)
401
402
SEMINARS IN NEUROLOGY/VOLUME 22, NUMBER 4 2002
Jean-Martin Charcot (1825 to 1893)
Charcot localized many of the motor centers of the cerebral cortex and was perhaps the first to describe syphilitic
and amyotrophic lateral sclerosis.31,32 In addition to these
contributions to the understanding of the motor system,
Charcot also made valuable contributions in approaching the examination of the senses. He demonstrated his
examination techniques during his “Tuesday Lessons.”
He tested superficial pain sensation by pinching, pricking, or electrically stimulating the skin. In addition to
using the Romberg sign (eyes open and closed) he developed a temperature perception device.32 Charcot used
a heated thermometer on the skin of his patients to test
temperature sensation. Movements of torsion and extension of the extremities tested deep position and joint
sensation (proprioception).32,33
Charles Sherrington (1857 to 1952)
Charles Sherrington created dermatomal maps of the
peripheral nerves in monkeys. In the last decade of the
19th century he carefully studied the skin dermatomes
supplied by the dorsal root ganglia. Sherrington cut the
dorsal roots of monkeys above and below specific spinal
levels, demonstrating areas of sensibility that corresponded to specific and intact nerve roots. Sherrington
found smaller territories of spinal roots for pain and
temperature than for touch.34 Importantly, he also demonstrated axon branching and showed that the axonal
pain pathways were proof of an organized sensory network.6,35,36 Sherrington noted that his work in animals
was strikingly similar to his friend and fellow poet Henry
Head’s work on human dermatomes.
Sir Henry Head (1861 to 1940)
Sir Henry Head’s experiments increased our understanding of the sensory system and enhanced our ability to
examine it.5,37–41 Frustrated with the inconsistent reports of patients with sensory loss, he performed his most
famous experiment in which he severed his own radial
nerve and documented the return of sensory modalities.5,42 This experiment, however, was not his major
contribution to our understanding of the sensory examination. After years of experiments on sensory nerves,
Head began to piece together a possible organization for
the sensory afferent system. He divided the peripheral
nervous system into three distinct sensibilities: deep,
protopathic, and epicritic. He described deep sensibility
as being served by fibers that ran mainly with muscular
nerves. They were concerned with pressure stimuli as well
as with joints, tendons, and muscle movement. Protopathic sensibility was described as that which was “capable of responding to painful cutaneous stimuli and
extremes of heat and cold.”5 Protopathic pain was generated in the posterior nerve root and exhibited the
highest threshold for a pain response with poor localization, failure to adapt, and intense response to stimulation. Epicritic sensibility was the ability to discriminate between two points and to recognize fine grades in
temperature change. Head believed it was more precisely tuned than protopathic sensation. Head correctly
surmised that epicritic pain fibers were distributed
throughout the peripheral nervous system and had
slower regeneration times.5,43–45
Another important contribution Head made was
to map the human dermatomes.5,46 Before he developed
his drawings, the dermatomes were simply referred to as
pain spots.4,36 Through his human research, he was able
to construct an accurate depiction of all the nerve dermatomes in the peripheral nervous system. Using patients with herpes zoster, he mapped their rashes to specific dermatome segments and correctly noted that they
were confined to an afflicted spinal root.47 Head mapped
the dermatomes using the information he had accumulated on the dorsal root ganglia, which was known to
supply sensation to specific regions of the skin. Using
herpes zoster as a model, Head was able to determine
sets of dermatomes and match them with specific spinal
roots.46
Otfrid Foerster (1873 to 1941)
Otfrid Foerster, through his 30 years of carefully mapping the human dermatomes, was able to demonstrate
overlap in nerve distributions. This was an important observation; although correct, this conflicted with Head’s
studies. Foerster tested for residual sensibility in his patients by utilizing vasodilatation and electrical stimulation of the peripheral end of a severed posterior nerve
root.36,48 Additionally, Foerster suggested the concept of
gate control. This theory put forth the idea that large
nerve fibers could inhibit small nerve fibers during a
painful experience.7,48 He also introduced topographical
localization of function, suggesting that pain fibers
were in different locations from temperature and touch
fibers.4,48
Herbert Gasser (1888 to 1963) and
Joseph Erlanger (1874 to 1965)
Luigi Galvani (1737 to 1798) was a physiologist from
Bologna, Italy who discovered that a dissected frog’s leg
would twitch when touched with a metal scalpel. While
investigating the effects of electrostatic stimuli applied
to the muscle fiber of frogs, he discovered he could make
the muscle twitch by touching the nerve with various
metals that did not have a source of electrostatic charge.
He also noted that there was a larger reaction if two dissimilar metals were used. He called this the animal’s
electricity.49 Alessandro Volta (1745 to 1827) was an
Italian scientist and inventor. In 1775 he introduced his
ORIGINS OF THE SENSORY EXAMINATION/FREEMAN, OKUN
first important invention, the electrophorus. The device
was capable of passing an electric charge to another object. Following up on the experiments of Luigi Galvani,
Volta studied animal electricity; Volta’s “voltaic pile”
provided proof that electricity could be conducted
through and produced by nonorganic matter. Volta had
introduced the battery (Fig. 2). Galvini and Volta paved
the way for further studies of nerves in humans.
Building on Weber’s 1847 idea that cold could
inhibit nerve conduction,50 Joseph Erlanger and Herbert
Gasser set out to determine what kind of effect local
anesthetics would have on nerve fibers of differing
sizes.1,51 In 1929 at Washington University they used
both the application of pressure as well as cocaine to block
nerve fiber conduction in frogs.51,52 Their observations
were integral in developing the understanding of how
nerve conduction could be blocked and how techniques
could be used to decipher stimuli with regard to particular nerves. The two investigators determined that fiber
size was the dominant factor in the production of sensory dissociation.4,52 They also analyzed the relationship
of nerve and nerve fiber properties to conduction rate
and electrical threshold.51,52
Erlanger and Gasser performed nerve conduction velocity studies in 1924.51 The device they invented
utilized a cathode ray tube and oscillograph to demonstrate action potential peaks of three different types of
nerve fibers. Based on that data they were able to deduce that all nerve fibers would not conduct impulses at
the same time; furthermore, the fibers carried different
types of sensory information.51
Figure 3 Von Frey hairs. Through the use of a camel hair, various levels of pressure are applied to the skin and pressure is
calculated. The hair is mounted inside a tube. Calculations are
made respective to how much the hair is bent during the examination.66
Max von Frey (1852 to 1932)
In 1895 Max von Frey introduced the specificity theory
of sensation. He postulated that heat, cold, touch, and
pain were the four specific modalities for sensation. Von
Frey believed that the skin receptors were differentiated
by a “lowest threshold for energy” phenomenon and that
specific skin receptors subserved specific sensations. The
examination of touch could be tested with what became
known as von Frey hairs, which were bristles of hair
(horse hair) of varying thickness (Fig. 3).3,30 The hairs
were pressed against the skin until they bent. They were
previously calibrated with a balance so the force to bend
them was already charted.3 Today, nylon fibers are used
to perform the same task.53
in his text that “each form of sensation, of touch, temperature, and pain, must be separately tested, since one
may be affected and not another.”11 By 1920 there were
four principle functions tested during the sensory examination including (1) tactile sensibility, (2) temperature
sensation, (3) pain sensation, and (4) deep sensibility.54
Bing’s Compendium, a leading source of examination information at that time, described tests for the different
sensibilities. Tactile sensibility was tested with cotton
wool, a camel-hair brush, or a finger. A depleted tactile
sense was called tactile hypesthesia, and absence of sensation was termed tactile anesthesia. Temperature was tested
by determining the ability to differentiate between warm
and cold. According to Bing’s Compendium there was no
specific tool for investigation,54 although Charcot had
utilized a heated thermometer in the 1800s.32,33 Pinprick and pinching were both suggested as tests for sensibility to pain (superficial sensibility), and for the first
time the sensibilities were now separated into protopathic and epicritic as a result of Henry Head’s important observations in the first two decades of the 20th
century.5 Deep sensibility was tested by flexion and abduction of limbs and joints as well as with a new addition to the neurologist’s instruments of examination,
the tuning fork.54,55 All of the above were commonly
found in a doctor’s medical bag.54
In the 1970s Peter Dyck and colleagues developed
another method for testing sensation. They used an automated system to test touch-pressure, vibratory, and thermal sensation. The system had 21 stimulus levels and
scoring was accomplished by a computer.53 Although this
was a novel device, it did not find widespread use as traditional bedside methods of the sensory examination
proved adequate for most neurological diseases.
DEVELOPMENT OF THE
NEUROLOGICAL EXAMINATION
In 1888, A Manual of Diseases of the Nervous System was
published by W.R. Gowers11; in it was one of the first
complete sensory examinations. It detailed tests for tactile, thermal, and pain sensation but did not include an
examination for vibratory sensation.22 Gowers remarked
Pain/Tactile Sensation and the Pin Prick Test
In examining tactile sensibility Gowers in 1888 described
an examination that is remarkably similar to the modern
sensory exam. “In examining the tactile sensibility, it is
important to ascertain, not only whether the patient
can feel, but whether he is able to recognize the place
403
404
SEMINARS IN NEUROLOGY/VOLUME 22, NUMBER 4 2002
touched—whether he can correctly localize the sensation. For this he must be asked not only whether he
feels the touch, but to say or point out where he feels it.
The part touched should be frequently varied, and the
eyes, of course, kept closed.” Gowers went on to describe sensibility to pain as:
subserved by what are called nerves of common
sensibility. It may be tested by prick or pinch. For a
prick, too fine a point must not be used, not only because a sharp point may inflict a needless wound, but
because, in the less sensitive parts of the skin, where the
terminal nerve plexus is wide, a fine point may here or
there be unfelt, although it penetrates the skin. Hence a
somewhat blunt point should be employed. Nothing
answers better than the point of a quill pen.11
Gowers also warned his readers that the practical value of
the tests may be less than anticipated, as interpretation of
findings on the sensory examination was difficult.11
It was postulated in the 19th and 20th centuries
that lesions in the posterior columns of the spinal cord
rather than the spinothalamic tract would impair tactile
sensibility, and an interruption of the posterior and lateral columns would completely abolish tactile sensation.54 Additionally, it was erroneously felt that the pyramidal tract and other descending pathways played a role
in production of pain.54,56 Pinprick testing during this
time period proved an excellent way to localize pain and
led Erlanger, Gasser, and others to perform localized
nerve blocks.51 Much of the research gleaned from nerve
blocking contributed to the development of local anesthesia.36
Dermatome experiments by Henry Head46 and
Otfrid Foerster48 had a tremendous influence on how
the pinprick examination was performed. Since a new
map of the human dermatomes was created, pinprick
tests could be done on specific nerve levels and dysfunction traced to a single dorsal root. This made the test
more effective and specific in diagnosis.
The pinprick test was also utilized proximally and
distally on body parts by Gordon Holmes, who found
this useful for localization.57 Ernst Weber previously
used a similar technique for localization by applying
varying amounts of pressure.58 Weber also went on to
describe the two-point discrimination test in which he
utilized a compass to examine whether patients could
perceive how far away two simultaneously applied stimuli occurred on the skin.58
Temperature Sensation
Temperature sensation was classically divided into hot
(40 to 45°C) and cold (5 to 10°C).54 Specific values
were used because examiners realized that higher or
lower temperatures had the propensity to elicit pain
responses rather than the desired change in temperature.
Examiners chose metal for testing this sensation because it served as an excellent conductor of heat.1 Testing was performed after metal rods were heated or cooled
to an appropriate temperature and then applied superficially to the skin.1 While it was discovered that sensory nerve endings were not entirely specific for heat
or cold, they could detect changes in temperature.
Gowers suggested in his textbook that “for course examination, hot and cold spoons may be employed; for
ascertaining the power of differential discrimination,
test tubes, containing water at different temperatures
are necessary.”11 For practical purposes Gowers remarked
that the result was “hardly commensurate with the time
required for the examination.”11 Additionally, as pain
and temperature fibers were closely associated, lesions
of the spinothalamic pathways were found to affect
both pain and temperature. Disturbances of temperature
sensation were referred to as thermanesthesia, thermhypesthesia, thermhyperthesia, and isothermagnosia (the perception that all temperatures are warm) in the case of
higher spinal cord injury.1
Charcot was known to use a thermometer that
could be heated or cooled and placed carefully on a patient’s skin.32 This clever method of examination was
utilized to ensure that the patient skin would not be
damaged. Charcot used clinical thermometry to determine differences in the fevers of hysteria and epilepsy.
He showed epilepsy patients suffered potentially lifethreatening elevations in temperatures, and hysteria patients could sustain several clinical attacks in a single
day without a significant change in body temperature.33
Additionally, temperature sense was found to vary among
body parts. Sensibility to cold was least in the epigatrium and sensibility to heat least on the back, while
heat and cold were found to have the greatest sensitivity
on the knee.11
Two-Point Discrimination and the Compass
Two-point discrimination was described as the differentiation between two points placed at variable distances
on the skin. A compass or two-point esthesiometer
could be used for the two-point discrimination test
(Fig. 4). Ernst Weber, a German physiologist, was one
of the first scientists to develop tests examining cutaneous sensation. In 1846 he published a chapter in
Rudolph Wagner’s book, Handwoerterbuch der Physiologie.58 In the chapter he described his two-point discrimination test, performed with a compass, as well as
his tactual test performed with a blunted tip covered in
charcoal. Additionally, Weber described how discernable differences in the pressure of stimuli increased with
a fractional increase of the weight of stimuli, a principle later termed Weber’s law.58 Weber’s work in this
area, which included the development of the bedside
ORIGINS OF THE SENSORY EXAMINATION/FREEMAN, OKUN
Figure 4 Ebbinghaus-style esthesiometer. Similar to the twopoint device employed by von Frey, this esthesiometer utilized
ivory points as the “hairs.”66
test for two-point discrimination, was influential in the
study of tactile physiology. Later, in 1927, Gordon
Holmes described the use of the compass on cortical
lesions that caused sensory loss.57
Holmes felt that Weber’s compasses were underutilized in clinical practice, especially in lesions of the
cortical sensory zone. He frequently noted that the compass test provided a valuable sign for the localization of
cortical lesions. He found that in two cases of endotheliomas of the falx and in one case of glioma the compass
test provided the only localizing sign. He observed in one
of these three cases, “on the dorsum of the left foot she
was always correct when the points were separated by 3
cm, but on the right foot she frequently failed to recognize them, even when they were 5 cm apart. In this case
there was no defect of the sense of position or of movement, nor disturbance of any other form of sensation.57
Vibratory Sensation and the Tuning Fork
The astrologer, physician, and mathematician Cardano
in 1550 proposed that sound could be transmitted
through the bony skull and air.22 Capavacci, a physician
in Padua, utilized Cardano’s idea to differentiate between middle ear and nerve deafness.59–61 The modern
tuning fork was constructed in 1711 by the trumpeter
and lutist John Shore. It was utilized as an instrument
that, when vibrated, produced a note of constant pitch.
In 1546, Giovanni Felippo Ingrassia of Italy discovered
bone conduction by observing that a vibrating fork could
be heard when pressed against the teeth. Later, in 1864,
Friedrich Rinne used the tuning fork to compare air and
bone conduction in the diagnosis of deafness.24
The tuning fork (Fig. 5) test for vibration sense
was developed by Heinrich Rumpf in 1889.25 Tomson
and others argued that vibration was a discrete sensation
that was sometimes impaired when touch and pressure
were preserved, while Egger held that the receptors were
in the periosteum and the sensation was conducted by
bone.62 The test was not considered valid until the early
20th century when it was agreed that vibration was a
discrete and testable examination finding, after which it
began to appear in European books such as Lewandowsky’s Handbook of Neurology55 and the American
book Bing’s Compendium of Regional Diagnosis.54 In the
1920s it was suggested that the tuning fork be placed on
“superficially situated parts of the bony skeleton.”54 The
fork provided both the appropriate amplitude and frequency of mechanical displacement. The examination
was performed by holding the tuning fork over a joint or
bone while letting it vibrate at 128 Hz. The bone would
act as a resonator and convey vibratory sensations through
the skin and subcutaneous tissue. The patient would respond to the examiner, noting either when the vibration
stopped or whether there was a decrement in vibratory
sensation when compared with the opposite side of the
body. Tests could be performed in various places including the wrist, the sternum, the clavicle, or on the extremities. The experienced examiner noted the gradients of change between proximal and distal body parts.1,54
The loss of vibratory perception was referred to as pallanesthesia.1,30
Proprioception
When bedside proprioceptive tests other than the
Romberg sign were introduced is unclear. Charcot had
observed patients who had difficulty with limb posturing and limb positioning, but it is not clear that he was
the first to describe and test this phenomenon.63 Although proprioceptive receptors were described by
Kuehne in 1878,64 the concept of proprioceptive function could be credited to several 19th century investigators, including Ferrier and Sherrington.6,35,65
Between 1840 and 1846 Moritz Heinrich Romberg published in Lehrbuch der Nerven-Krankheiten des
Menschen what he considered to be a diagnostic sign for
tabes dorsalis.17 His test, which was essentially a test of
B
A
Figure 5 (A) The modern tuning fork first used for the examination of the senses in 1889 by Rumpf is essentially the same tuning
fork employed centuries before by musicians, as well as for hearing tests. (B) Scientists also used the same tuning-fork technology
in 1867 to record reaction times.
405
406
SEMINARS IN NEUROLOGY/VOLUME 22, NUMBER 4 2002
conscious proprioception, called for the patient to stand
with eyes open and eyes shut in front of an examiner who
would evaluate body sway. When the patient swayed
with the eyes closed, a lesion of the posterior columns of
the spinal cord was suspected.17 The Romberg test was
more qualitative than quantitative. More complex devices,
such as Charles Dana’s ataxiagraph, have been subsequently introduced to more carefully document postural
sway.29 None of these devices have replaced the Romberg
sign, which remains a practical and easy method for diagnosis. The Romberg sign has since been standardized
but still has variability depending on the examiner. It remains one of the better signals of proprioceptive sensory
loss. Additionally, some have suggested to increase accuracy of testing for bilateral vestibular loss, acute unilateral vestibular loss, or pathology of the spinocerebellum, a sharpened Romberg test can be used. This
consists of narrowing the patient’s base of support by
placing feet in a heel to toe position or by standing on
foam rubber.29
CONCLUSION
Although not employed as a formal part of the neurological evaluation until the late 19th century, the origins
of the crucial aspects of the sensory examination date
back many centuries. Many important basic science discoveries and bedside observations led to important advances in the evaluation of the senses. Many aspects of
the historical examination remain practical and useful
in modern neurology.
ACKNOWLEDGMENTS
The authors would like to acknowledge the National
Library of Medicine for contributions and permission
to print original historical pictures. Additionally, the
authors would like to acknowledge Professor Thomas B.
Perera of Montclair State University for permission to
reprint pictures from his excellent website (http://www.
chss.montclair. edu/~pererat/telegrap.htm).
REFERENCES
1. Haerer A. DeJong’s, The Neurologic Examination. 5th ed.
Philadelphia: Lippincott; 1992
2. Mueller J. Handbuch der Physiologie des Menschen fuer
Vorlesungen. 2nd ed. Coblenz: J. Hoelscher; 1840
3. Frey MV. Beitraege sur Sinnesphysiologie der Haut. Saechsischen Akademie der Wissenschaften zu Leipzig. MathPhys Cl 1895;47:166–184
4. Sinclair DC. Cutaneous sensation and the doctrine of specific
energy. Brain 1955;78:584-611
5. Head H. Studies in Clinical Neurology. London: Hodder &
Stoughton; 1920:334–728
6. Sherrington C. The Integrative Action of the Nervous System. New Haven: Charles Scribner’s Sons; 1906
7. Foerster O. The motor cortex in man in the light of Hughlings Jackson’s doctrines. Brain 1936;59:135–159
8. Keele KD. Anatomies of Pain. Springfield: Thomas; 1957
9. Gowers WR. The Diagnosis of Diseases of the Spinal Cord.
London: J & A Churchill; 1880
10. Gowers WR. Lectures on the Diagnosis of Diseases of the
Brain. London: J & A Churchill; 1885
11. Gowers WR. A Manual of Disease of the Nervous System.
Vol. 1. London: Churchill; 1888:6–10
12. Brown-Séquard C. Experimental researches applied to physiology and pathology. Medical Examiner. Vol. 8. Philadelphia:
Baillière; 1852:481–504
13. Edinger L. Anatomie des Centres Nerveux. Paris: J.B. Bailliere et Fils; 1889
14. Edinger L. Einfuhrung in die Lehre vom Bau und den Verrichtungen des Nervensystems. Leipzig: F.C.W. Vogel; 1912
15. Gehuchten AV. Les Centres Nerveux Cerebrospinaux. Louvain: Uystpruyst-Dieudonne; 1908
16. Charcot J. Ataxie locomotrice progressive; arthopathie de
l’epaule gauche resultats necroseopiques. Arch Physiol Norm
Path 1869;2:121
17. von Romberg MH. Tabes dorsalis. Lehrbuch der Nervenkrankheiten des Menschen. Vol. 1. Berlin: Duncker; 1846:795
18. von Romberg MH. In: Sieveking EH, ed., trans. Lehrbuch
der Nervenkrankheiten des Menschen. London: Sydenham
Society; 1853 [AMotNDoM volumes]
19. Bell C. On the nervous circle which connects the voluntary
muscles with the brain. Phil Trans (part 2) 1826;116
20. Goldscheider JKAEA. Die spezifische Energie der Temperaturnerven. Mh Prakt Derm 1884;3:225
21. Goldscheider JKAEA. Neue Thatsachen uber die Hautsinnesnerven. Arch Anat Physiol Abt Supll 1885:1
22. Pearce JM. Early days of the tuning fork. J Neurol Neurosurg
Psych 1998;65:728–733
23. Ng M, Jackler RK. Early history of tuning-fork tests. Am J
Otol 1993;14:100–105
24. Rinne F. Rinne, Friedrich Heinrich. Beiträge zur Physiologie
des menschlichen Ohres. Beiträge zur Physiologie des menschlichen Ohres. Leipzig and Heidelberg: Zeitschrift für rationelle Medicin; 1864:12
25. Rumpf H. Ueber einen Fall von Syringomyelie nebst Beitrag
zur Untersuchung der Sensibilitat. Neurologisches Zentralblatt; 1889
26. Rydel A, Seiffer W. Untersuchungen uber das vibrationsgefuhl oder die sog. “Knockensensibilitat” (Pallasthesie). Arch
Psychol Nerven Krankheiten 1903;37:487–536
27. Hall M. Lectures on the Nervous System and its Diseases.
Vol. 27. London: Sherwood, Gilbert, Pyer; 1836
28. Brach B. Einige Worte ueber einen nicht hinlanglich
beachteten Punkt aus der Physiologie der Nerven und eine
eigenthumliche Art von Lahmung. Medicinische Zeitung
1840;9:215–217
29. Lanska DJ, Goetz CG. Romberg’s sign: development, adoption, and adaptation in the 19th century. Neurology 2000;55:
1201–1206
30. Pryse-Phillips W. Companion to Clinical Neurology. New
York: Little Brown and Company; 1995
31. Charcot J. Histologie de la sclérose en plaques. Gazette des
hôpitaux 1868;41:554–555
32. Charcot JRP. Les Démoniaques Dans L’art. Paris: A. Delahaye & E. Lecrosnier; 1887
33. Goetz CG, Bonduelle M, Gelfand T. Charcot: Constructing
Neurology. New York: Oxford University Press; 1995
34. Sherrington C. Experiments in the examination of the peripheral distribution of the fibres of the posterior roots of
ORIGINS OF THE SENSORY EXAMINATION/FREEMAN, OKUN
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
some spinal nerves. Philosophical Transactions B 1898;190:
45–186
Sherrington C. On the proprio-ceptive system, especially in
its reflex aspect. Brain 1906;29:467–482
Sinclair DC, Weddell G, Feindel WH. Referred pain and associated phenomena. Brain 1948;71:184–209
Head H, Rivers WHR. The afferent nervous system from a
new aspect. Brain 1911;28:99–115
Head H, Holmes G. Sensory disturbances from cerebral lesions. Brain 1911;34:102–254
Head H. Six clinical lectures on the diagnostic value of sensory changes in diseases of the nervous system. Clin J 1913;
40:337,358,375,396,408
Head H, Riddoch G. The automatic bladder, excessive sweating and some other reflex conditions in gross injuries of the
spinal cord. Brain 1917;40:188–263
Head H. Special Report Ser Med Research Council 1918;28
Head H, Rivers WHR. A human experiment in nerve division. Brain 1908;31:323–450
Henson RA. Henry Head’s work on sensation. Brain 1961;
84:535–539
Henson RA. Henry Head: his influence on the development
of ideas on sensation. Br Med Bull 1977;33:91–96
Henson RA. Henry Head: man of culture, compassion and
science. J Med Biogr 1998;6:15–20
Head H, Campbell AW. The pathology of herpes zoster and
its bearing on sensory localization. Brain 1900;23:353–523
Head HT. The grouping of afferent impulses within the
spinal cord. Brain 1906;29:537–541
Foerster O. The dermatomes in man. Brain 1933;56:1–39
Boller F, Keefe NC, Zoccolotti P. Luigi Galvani, body electricity and the galvanic skin response. Neurology 1989;39:868–870
Weber HD. A Contribution to the Pathology of the Crura
Cerebri. London: Medico-Chirurgical Transactions; 1863,46:
121–139
Erlanger J, Gasser HS. The compound nature of the action
current of nerve as disclosed by the cathode ray oscilloscope.
Am J Physiol 1924;70:624
Gasser HS, Erlanger J. The role of fiber size in the establishment of a nerve block by pressure or cocaine. Amer J Physiol
1929;88:581–591
53. Dyke P, et al. Automated system to evaluate sensation. Annals
of Neurology 1978;4:502–508
54. Bing R. Compendium of Regional Diagnosis in Affectations of the Brain and Spinal Cord. 3rd Ed. St. Louis: F.S.
Arnold; 1929
55. Lewandowsky M. Handbuk ser Neurologie. Bd 1. Allg. Neurologie 11. Berlin: Springer; 1910:499–502
56. Bloedel JR, McCreery DB. Organization of peripheral and
central pain pathways. Surg Neurol 1975;4:65–75
57. Holmes G. Disorders of sensation produced by cortical lesions. Brain 1927;50:413–427
58. Weber E. Ueber die Gestalt des Gehirns der Schleie, Cyprinus tinca, im Alter von einem Jahr und bei dem erwachsenen Thiere. Berlin: Arch Anat Physiol wissen Med; 1846:
478
59. Feldmann H. [History of the tuning fork. III: On the way to
quantitative pure-tone measurement. Pictures from the history of otorhinolaryngology, represented by instruments from
the collection of the Ingolstadt German Medical History
Museum]. Laryngorhinootologie 1997;76:428–434
60. Feldmann H. [History of the tuning fork. II: Evolution of the
classical experiments by Weber, Rinne and Schwabach].
Laryngorhinootologie 1997;76:318–326
61. Feldmann H. [History of the tuning fork. I: Invention of the
tuning fork, its course in music and natural sciences. Pictures
from the history of otorhinolaryngology, presented by instruments from the collection of the Ingolstadt German Medical
History Museum]. Laryngorhinootologie 1997;76:116–122
62. Egger M. CR Soc Biol Paris 1898;50:815–817
63. Charcot J, Pitres JA. Les Centres Moteurs Corticaux Chez
l’Homme. Paris: Rueff & Cie; 1895
64. Kuehne W. Ueber den Sehpurpur. Heidelberg: Untersuchungen physiologisches Institut; 1878:15–103
65. Ferrier DT. An experimental research upon cerebro-cortical
afferent and efferent tracts. Proc Roy Soc Lond 1901;62:
1–3
66. Zimmermann E. Preis-Liste über psychologische und physiologische Apparate. Leipzig: 1903:114
407