The tortuous path of the plantar response: A tedious argument
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/0028-3886.190256
Source of Support: None, Conflict of Interest: None
It is generally accepted that Joseph Juan Felix François Babinski (1857–1932) of Paris, France, described the plantar response. This is true in a large measure, and very few shall raise serious questions about Babinski's primacy in terms of describing the sign; however, the story is much more convoluted and it certainly demands a detailed study.
Aretaeus of Cappadocia, a Greek physician, who presumably described diabetes mellitus for the first time, wrote in about 1500 AD, “If, therefore, the commencement of the affection be below the head, such as the membrane of the spinal marrow, the parts which are homonymous and connected with it are paralysed; the right on the right side and the left on the left side. But if the head be primarily affected on the right side, the left side of the body will be paralysed; and the right, if on the left side. The cause of this is the interchange in the origin of the nerves, for they do not pass along on the same side, the right on the right side, until their terminations; but each of them passes over to the other side from that of its origin, decussating each other in the form of the letter X.”
The idea, thereafter, was shelved for nearly 1700 years and nobody took any serious notice, even though painters of the Medieval, Renaissance, and Baroque periods, such as Sandro Botticelli (1445–1510), and Raphael (1483–150), from Italy, painted the infant Jesus in mother Mary's arm, portraying an upgoing toe on tickling the sole. Carl Wernicke (1848–1905), of Germany, revived the forgotten concept and reported dorsiflexion of the toe in a case of hemiparesis in the late 19th century, and a few years later, Adolf Gustav Strümpell (1853–1925), also from Germany, described the same phenomenon in amyotrophic lateral sclerosis, even though they did not report the implication of the sign.,, In 1893, Ernst Julius Remak (1849–1911), a German physiologist, described the extensor plantar response in a patient with transverse myelitis and wrote,“One is able, through stroking of the distal half of the plantar aspect of the metatarsus primus, to evoke a fairly isolated reflex of the extensor hallucis longus.”
On the 22nd of February, 1896, Joseph Babinski presented a brief paper, entitled, “Sur le réflexe cutané plantaire dans certains affections organiques du système nerveux central,” literally meaning, “On the cutaneous plantar reflex in certain organic disorders of the nervous system” before the Société de Biologie, the forerunner of the French Neurological Society, in Paris and drew attention to the up going toe. Lively clinical meetings were regularly held there and Jean-Martin Charcot (1825–1893) presented his early cases of amyotrophic lateral sclerosis, Guillaume-Benjamin-Amand Duchenne de Boulogne (1806–1875) expressed his ideas about muscular dystrophy, and Paul Broca (1824–1880) described the case of “Tan,” his first case of non-fluent aphasia before an erudite gathering. James Jackson Putnam (1846–1918), an American neurologist, happened to be present in one such meetings and wrote,
“This afternoon, he took me to the séance of the Société de Biologie, where all the swells make reports. Claude Bernard, a fine-looking old man in a velvet cap and fur-trimmed coat, presided, and Charcot and Vulpian and Ranvier all had their say, of which I understood more or less…For all their French blood, the members behaved a good deal like schoolboys, and for all the rings of his bell, M. Bernard couldn't keep the room quiet.”
On the cutaneous plantar reflex in certain organic disorders of the nervous system
Babinski's paper was a model of clarity of thought and brevity of expression. It was the outcome of an extraordinary power of observation, tinctured with clinical acumen of the highest order. Robert Wartenberg once remarked, “In its simplicity, clinical importance and physiological implications, the Babinski sign has hardly an equal in medicine.” He did not describe the upward movement of the great toe as the most important component of the reflex. On the contrary, he stressed that all the toes were extended while the foot was pricked. In addition, it is not clear from his writing whether he stimulated the foot once or several times, and the part of the sole which he preferred. He also observed that all the patients with an up going toe had weakness of the ipsilateral lower limb. It was only in his second paper in Semaine Médicale in 1898 that he emphasized the extension of the hallux with strong and nociceptive tactile stimulation such as stroking of the lateral border of the sole. He observed that pricking the hemiplegic limb on the sole leads to extension of the great toe at the metatarsophalangeal joints even in patients who had lost their power of moving the limbs completely. The paper contained no reference nor was there any mention of the number of patients he studied. Kumarand Ramasubramanian feel that it was most unlikely that Babinski ever read the paper of Ernst Julius Remak since he wrote in first person “I have observed in some cases,” and the language suggested the kind of tenor that he was the first person to observe the sign. However, his subsequent paper in 1903, reads somewhat differently and he writes, “Stimulation of the sole of the foot sometimes provokes, among other reflex movements, an abduction of one or more toes. This response has been described incidentally by other authors who did not attach any semiologic value to it,” thus, clearly indicating that he was, by this time, conversant with Remak's work. He further wrote that healthy patients, “show the response rarely and when it exists is slight.”
Subsequent workers found little substance in Babinski's pronouncement, and observed that the specificity of plantar response is nearly 100%., Estapol et al., studied 100 patients with hemiplegia or paraplegia and observed that Babinski sign was negative in 16% of these cases. Babinski called the sign, “phenomenon des orteils,”meaning “phenomenon of the great toe,”,, and stated that the response was best noted in the first two toes and observed in hemiplegia, paraplegia, and in Friedreich's ataxia. He attributed the sign to the dysfunction of the pyramidal tract, and pointed out that it was usually associated with exaggeration of tendon reflexes and clonic movements. He also noticed transient appearance of the sign following an attack of Jacksonian fit and strychnine poisoning, and emphasized that the sign was not found in hysterical weakness. In his extremely brief paper in 1903, he remarked that abduction of the other toes or fanning was, at times, an accompanying feature, and called it “le signe de l'éventail,” though others have attributed the discovery of this sign to Duprê.,, In this paper, he made the very important observation that the sign could not often be elicited in acute paraplegia or hemiplegia with normal, diminished, or even absent stretch reflexes, and that the dorsiflexors of the ankle were weak. In a patient with a history of stroke for 24 hours, he found the up going great toe, while the stretch reflexes were of equal intensity on both the sides. Finally, in a patient who sustained a cerebrovascular attack only 1 hour ago, the plantar response was extensor; however, the stretch reflexes were hypoactive., In two patients with spinal transection, one appearing 9 hours and the other after 3 hours, there was no movement of the great toe, and it has been postulated that in all likelihood, it represented profound depression of the polysynaptic flexor response. Babinski ended his paper with an important conclusion that it could be used in medicolegal practice to differentiate between organic paralysis and malingering, as he himself had done in a case of paraplegia following road traffic accident, and ended his paper with the cautionary note, “…a sign of probability in favor of a dysfunction of the pyramidal system. This can be valuable in certain doubtful cases” clearly indicating that it may not be present in each and every case of pyramidal tract damage., One cartoon appeared in the popular tabloid, Chanteclair, which portrayed Babinski stroking the left sole of a subject with his right index finger, and the toes are held in an extended and abducted posture. A hand fan with a swan in the middle and a hammer lying by his side tells the entire story.,
Babinski made his observations drawing from the works of George Prochaska (1749–1820), of Czechoslovakia, who carried out pioneering experiments on the flexor mass reflex, which was interpreted as a spinal reflex by Marshall Hall (1799–1857). This is an abnormal condition, seen in patients with transection of the spinal cord and characterized by a widespread neural discharge. Stimulation below the level of the lesion results in flexor spasms, sphincter incontinence, priapism, hypertension, and profuse sweating. Though Babinski categorically attributed the up going great toe to dysfunction of the pyramidal tract, Nathan and Smith studied a cohort of patients and observed that lesions located in the anterior part of the spinal cord, which spared the corticospinal tract, may occasionally be associated with an extensor plantar response, while sometimes, it may not be seen following definite damage to that tract. Landau and Clare felt that interruption of the internuncial non pyramidal neurons may facilitate the release phenomenon, and the plantar response may be extensor, even if the pyramidal fibres were spared, while Lundborg asserted that concomitant damage to the corticospinal tract led to the appearance of the extensor plantar response. Its absence in hemiplegia suggests integrity of these tracts., In 1960, Kugelberg et al., provided the neurophysiological basis of this reflex on the basis of electromyographic studies and suggested that each area of the body has a specific reflex response to nociceptive stimulus, and the purpose of the reflex was to withdraw the anatomical area from the noxious agent as a protective phenomenon. The reflex is mediated at the level of the spinal cord and influenced by inputs from higher centers such as the corticospinal tract. Such a stimulus applied to the sole causes prompt flexion of all the joints in the lower limb. Simultaneously, as suggested by Grimby, one more reflex, the great toe reflex, mediated by stimulus on the ball of the great toe by a noxious stimulus operates, which causes extension of the great toe but flexion of other lower limb joints. Thus, the extensor plantar reflex is an abnormal response following stimulation in the “wrong receptive zone.” There is recruitment of the extensor hallucis longus along with overpowering of the flexors of the toe.
For a long time, it has been known that the extension of the great toe is actually a flexor response in terms of physiology and a vice-versa penomenon occurs during plantar flexion.,,,, As already stated, stimulation of the great toe by pinprick induces extension of the great toe in normal individuals, and this field extends in pathological conditions to the 1st sacral dermatome, or even further. In some cases, the reflexogenic zone for the Babinski response may extend beyond the lateral aspect of the sole to the leg or the thigh, or even higher, after an acute cerebral insult, and stimuli of lesser nociceptive magnitude may result in the response. This phenomenon has been used by many neurologists to suggest alternate methods of eliciting the plantar response soon after Babinski's paper appeared. The subject aroused a lot of interest, a number of papers started appearing in the medical literature;,,,,,, and Hermann Oppenheim (1858–1919) of Germany, described the sign by pressing down the anterior border of the tibia, Charles Gilbert Chaddock (1861–1936) of United States of America, by scratching the skin below the lateral malleolus of the fibula, Alfred Gordon (1874-–953) of France, by pressing the lower calf muscle, Paul Robert Bing of Switzerland (1878–1956), by multiple stimuli over the dorsolateral surface of the foot, Max Schaeffer (1852–1953) of Germany, by squeezing the tendoachilis, Erwin Stansky (1877–1962) of Austria, by a vigorous adduction of the little toe to be followed by sudden release, Antonio Egaz Moniz (1874–1955) of Portugal, by forceful passive flexion of the ankle, and many others.,, Van Gehuchten of Belgium, however, independently published his observations on this reflex, and Babinski sent him a piquant letter claiming his primacy in regard to its description. Gehuchten, in his magnanimity, accepted Babinski's view, and in his graciousness, preferred to call it “Babinski reflex.” For some unknown reasons, in the Netherlands, the reflex is known as the “Plantar response according to Strümpell.”, Babinski'sname appeared in the English language when James Stransfield Collier (1870–1935) of the United Kingdom wrote a paper in 1899 in the celebrated journal, Brain, where the photograph of the up going toe was also published. Collier called it “the extensor plantar response.”,, Oppenheim, on record, stated that he observed it long ago but found it rather fatuous and inconsistent for any tangible use. Two neurophysiologists, Eric Kugelberg (1913–1983), from Sweden, and John Farquhar Fulton (1899–1960), from the United States of America, provided experimental evidence from their work in chimpanzees that ablation of the motor cortex was associated with an extensor plantar response on the contralateral side.,
Babinski probably discovered his sign by serendipity. It was an observation by chance, and later, he replicated his finding. As he was instructed by Charcot, his mentor, to test each and every dermatome in patients with hysteria, the observation of the great toe going up in some cases and down in others, led him to use this sign to differentiate between an organic lesion and hysterical illness. As early as in 1896, he had the gumption to propose that the extensor toe was only a fragment of the more widespread flexor reflex synergy. It is now more or less accepted that the Babinski response is a modified part of the flexor reflex synergy, which appears when the polysynaptic flexor response is active.,, No wonder, Nathan and Smith wrote that “…it is probably the most famous sign in clinical neurology.”
Charles Gilbert Chaddock (1861–1936)
For a number of reasons, Chaddock's reflex merits independent treatment. He hailed from the United States of America, and elicited the identical response by scratching the skin below the lateral malleolus of the fibula in a semicircular fashion, and published his observations in an article entitled, “A Preliminary Communication Concerning a New Diagnostic Sign.” He wrote,,
“I have found that extension of one or more or all of the toes with or without fanning of them on irritation of external infra malleolar skin in cases of organic disease, is a spinal cortical reflex path. I shall call it the external malleolar sign.”
Chaddock was cautious, emphasized on proper relaxation of the lower limb, and used a dull steel point for scratching the skin. He found the sign in cases of fracture of the skull, in unilateral, or bilateral cerebral lesions, and in lesions of the spinal cord. He further wrote,,
“In order to justify such an assumption as my title indicates it is necessary to show that what I call a new sign has not been described to my knowledge; that it is an independent manifestation, elicited in a definite way, and capable of affording diagnostic evidence of importance; that it does not occur in health or in a haphazard fashion in disease; that for practical purposes it does not require a technique too complicated for routine application; and that its manifestation is clear enough for reliable interpretation.”
It is of some interest to know that Chaddock spent some time with Babinski while he travelled to France from 1897 to 1899. The few issues where Chaddock, in a way out-shone Babinski include his demonstration that in unilateral lesions also, one could observe both the great toes moving upwards on scratching, most probably due to the involvement of uncrossed corticospinal fibres and the sign described by him appeared and persisted even when Babinski's sign could no longer be elicited., Withdrawal responses were also less frequently observed. Importantly, he described an equivalent sign in the upper extremity as well. He propounded that stimulating the ulnar side of palmaris longus or flexor carpi radialis led to the rather abnormal response of wrist flexion with the fingers spreading, in involvement of the corticospinal tract. He classified his sign as slight, marked, and very marked. Chaddock leaned heavily on Babinski for review of his work and wrote about his method of eliciting the sign to him. Henri, Babinski's brother, wrote back that his brother found the reflex of particular interest, though it is to be noted that Babinski did not mention Chaddock's work in his subsequent writings. Interestingly, Henri sought his favor to popularize his brother's cookbook in the United States of America! He wrote,
“My brother asked me to let you know that he has verified your observation on the reflexes. He finds your works very interesting and would be delighted to discuss them when you visit Paris again.”,
Just as a number of neurologists described the up going great toe on scratching the lateral aspect of the sole before Babinski, Kisaku Yoshimura (1879–1945), a physician from Japan alluded to the external malleolar sign in 1906, five years before Chaddock. He wrote,,,
“The extension of the big toe may be obtained by stimulating the dorsal lateral aspect of the foot from the posterior portion of the skin beneath the external malleolus anteriorly along the external edge of the foot. In examining for Babinski's phenomenon, the stimulation of the dorsum should never be forgotten even if the stimulation of the sole provokes the flexion of the big toe.”
In no way does Chaddock's sign replace Babinski's response; on the contrary, the two signs are complementary. However, it is a common experience that in situ ations, when it is difficult to elicit the Babinski's response, for instance, on the thick soles particularly of farmers in a country like India (where the farmers walk bare feet), the Chaddock's sign is found positive without much difficulty. In 1986, Tashiro examined 13 patients and found that the Babinski response was present in 79%, whereas positive Chaddock's sign could be elicited in all of them, and in the process, observed an up going toe when the dorsum of the foot was scratched from the medial to the lateral side. He termed it the “reversed Chaddock's sign or Tashiro's sign.”, Some have suggested that both Babinski response and Chaddock sign are found in lesions in Brodmann Area 4, or the motor cortex, whereas lesions of the premotor cortex or Brodmann Area 6 and its descending fibres lead to fanning of the toes without a positive Chaddock's sign, even though the Hoffman sign and forcing grasping reflex are elicited. These have not been proved to be sacrosanct by other investigators, and Goetz provides the caveat that attempts at anatomical localization may be fraught with errors and the best way would be to treat these two signs as complementary to each other.
A number of studies have examined the reliability and reproducibility of the Babinski sign and the inter observer Kappa values have ranged from 0.15 to 0.57. However, the studies involved only a few candidates and there were considerable methodological variations. One study compared the usefulness of Babinski's sign with the related ones described by Chaddock, Gordon, and Oppenheimer, and observed that the Babinski sign had the best yield. Jaramillo et al., studied 107 patients and observed that the Babinski sign had a low sensitivity (50.8%, 95% confidence interval 41.5–60.1) but a high specificity (99%, 95%, confidence interval 97.7–100) in identifying pyramidal tract dysfunction.
Eliciting the Babinski's response properly is often taken as the benchmark of one's neurological perspicacity at the bedside. Some of those who described related signs later were truly ingenious, while others were somewhat vapid. Somebody even lionized himself by stating that ever since Babinski described the sign, neurology is standing on an upgoing toe! Purdy, among others, have felt that the Babinski sign is the most important clinical sign described in the entire gamut of clinical neurology because it is a tell-tale evidence of damage to a certain cerebrospinal tract, whereas Miller and Johnston have stated that it should be expunged from the neurological vocabulary owing to its inconsistency and somewhat overstated importance. As the use of eponyms are discouraged now-a-days, JW Lance raised the pertinent question, that we should abandon the term, “Babinski's sign,” in favor of “the up going toe” or “extensor plantar response,” as James Collier called it in 1899. After much deliberations, he declared that he would rather agree with what Robert Wartenberg, the famed American neurologist, once said, “By the great Babinski, no.”, And everything said, it brooks little argument that the palm goes unhesitatingly to Babinski for describing, arguably, the most incontrovertible sign indicating pyramidal tract damage.