- Email: [email protected]
The Babinski sign in sickness and in health
Clinical Chiropractic (2011) 14, 122—126
www.elsevier.com/locate/clch
LITERATURE REVIEW
The Babinski sign in sickness and in health Robin Pauc * The Tinsley House Clinic, Main Road, East Boldre, Hants, UK Received 16 September 2010; received in revised form 25 June 2011; accepted 6 July 2011
KEYWORDS Babinski; Babinski sign; Extensor plantar response; Neurological examination; Superficial abdominal reflex
Summary The Babinski sign is a well documented phenomenon and testing for its presence forms part of the standard neurological examination. However, although historically it is considered to indicate an upper motor neuron lesion related to pathology anywhere in the course of the corticospinal tract, it has been found to be present in healthy children, in adults, and in increasing numbers in the elderly population. It may therefore also be a sign of the state of development of the brain and its subsequent decline. Objective: To draw together research being conducted into the Babinski sign, how it should be performed, how it should be evaluated, its validity and possible falsepositive extensor plantar responses seen as a result of developmental delay in both children and adults. Design: This study was a review of the available literature retrieved from computerised databases, the world wide web and authoritative texts. Method: All the information on current and past research was gathered from a computerised literature search of MEDLINE, Science Direct, Cochrane Library, Science Citation Index, SCOPUS, CINAHL and the world wide web. The search terms used were Babinski, Babinski sign, extensor plantar response. # 2011 The College of Chiropractors. Published by Elsevier Ltd. All rights reserved.
Contents Introduction . . . . . . . . . . . . . . . . . . History . . . . . . . . . . . . . . . . . . . . . . Normal reflexive development . . . . The Babinski sign . . . . . . . . . . . . . . Evaluation of results and validity of Discussion . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . .
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* Fax: +44 01590 612432. E-mail address: [email protected]. 1479-2354/$36.00 # 2011 The College of Chiropractors. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.clch.2011.07.007
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123 123 123 123 124 124 125 126
Babinski sign in sickness and health
Introduction The Babinski sign is well known to both students and practitioners alike and testing for its presence forms part of the standard neurological examination performed on virtually every patient and yet over the years its validity has been questioned and to date no one has satisfactorily explained what are the necessary neurodevelopmental changes that must take place before the primitive response seen in infants is replaced by the adult form.1 It has been found to be present in a high percentage of children diagnosed as suffering from learning and behavioural disorders and in a number of patients otherwise lacking signs of corticospinal damage.2,3 It returns in a number of otherwise healthy elderly subjects and may therefore indicate a decline in mental function associated with age related neuronal loss and the onset of dementia.4
History Although the discovery of the sign is attributed to Joseph Felix Francois Babinski, it had previously been described by Robert Remak (1815—1867) and had been portrayed in medieval, Renaissance and baroque art as occurring in infants.5,6 Remak first described the extensor plantar response in 1893 describing the response he had noted in a patient with transverse myelitis as follows: ‘‘One is able, through stroking the distal half of the plantar aspect of the metatarsus primus, to evoke a fairly isolated reflex of the extensor hallucis longus’’.7 In 1896 Babinski published a preliminary report of just 28 lines on the ‘‘reflexe cutane plantaire’’ (cutaneous plantar reflex) in which he described the phenomenon of the toes — signe de l’eventail — an extension of all toes with noxious stimulation (pricking) of the sole of the foot.8 It was not until 1898 that he specifically described the extension of the hallux with strong tactile stimulation (stroking) of the lateral border of the sole.9 In a third paper published in 1903 Babinski stated that if others had described the abnormal reflex before him they had found it fortuitously and did not realise its semiologic value.10
Normal reflexive development The plantar grasp reflex, a rudimentary response essential to infant apes in arboreal life, is considered to be one of the most primitive of the primitive reflexes and can be elicited in all pre-
123 term infants from 25 weeks of postconceptional age and continues to be present until 6 months postnatally. It is elicited by applying pressure to the sole of the foot just behind the toes. The infant should be placed in the supine position, must be awake and have the head in the midline position to avoid evoking an asymmetric tonic neck reflex. It is tonic in character and persists for 15—30 s following initiation.11 The plantar reflex is obtained by stroking the lateral aspect of the plantar surface of the foot from the heel towards the toes and then across the foot towards the medial aspect avoiding the flexor tendons and the ball of the great toe. The usual dominant response is that of plantar flexion of the toes and foot. The reflex is innervated by the tibial nerve (fourth lumbar through first or second sacral segment). This superficial reflex should be established by 12—18 months replacing the more primitive reflexive response of an extensor plantar seen in infants before this age.12 The timing of the change from the infantile to adult response has been related to the onset of walking.13
The Babinski sign The testing of the plantar reflex is a pivotal part of the standard neurological examination and the Babinski sign or response has been considered for many years to be the sine qua non among the pathological reflexes indicative of corticospinal tract lesions of the cortex, subcortex, brainstem or spinal cord.14 The sign itself consists of dorsiflexion of the big toe by recruitment of the extensor hallucis longus muscle following stimulation of the lateral aspect of the sole of the foot with a blunt object. Babinski himself noted the relationship between this sign and the shortening of other leg musculature as part of the flexion synergy of the lower limb.15 Care must be taken when testing the plantar reflex not to cause frank pain which may elicit a defensive withdrawal response which may be confused with a flexor reflex afferent response often found with a unilateral Babinski sign.16 Historically, the Babinski sign was the failure of the platysma muscle to contract on the side of a hemiparesis as described by Babinski in 1905.17 However, with time the eponym for the ‘‘great toe sign’’ of Babinski has stuck and is now firmly established as the name applied to dorsiflexion of the great toe with or without fanning of the other toes and withdrawal of the leg on plantar stimulation in patients with lesions of the corticospinal tract.
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Evaluation of results and validity of the Babinski sign In an ideal world the examination process should confirm the diagnostic impression and the Babinski sign would be present or absent. However, the Babinski response can be equivocal and information gleaned from the consultation and examination may bias an equivocal response towards being Babinski positive or absent.18 In a study of thity-four patients the inter- and intra-observer consistency of the Babinski reflex and its variants — Gordan, Chaddock and Oppenheim reflexes — were assessed following the examination of the patients by six neurologists. The Babinski reflex had the highest interobserver consistency with a kappa value of 0.491, while the Chaddock, Oppenheim and Gordon reflexes had kappa values of 0.4065, 0.3739 and 0.3515, respectively. The Babinski and Chaddock signs together have been found to be the most reliable tests for the lower limbs. The authors concluded that the Babinski reflex was the most consistent reflex between examiners but that the small sample size limited the conclusions that could be drawn from their results.19 In a second study the validity of the Babinski reflex was assessed again using the interobserver method (five neurologists and five non-specialists) and it was found that the reliability and validity of the Babinski reflex was fair with a kappa value of 0.30 but that foot tapping was substantially more reliable with a kappa value of 0.73. Again, the small sample size of just ten subjects must be taken into consideration as with the previous interobserver study.20 An evaluation of the reliability and validity of the Babinski reflex in a psychogeriatric population found that the response sets did not occur at random (P < 0.001) but that the reproducibility was so low that its clinical value in this elderly population was seriously questioned.21 This is somewhat surprising as in other studies it has been found to occur with greater frequency in both a healthy elderly adult population and in association with the onset of dementia.4 The reproducibility of the Babinski sign was assessed using 24 physicians and 12 patients again by means of the intraobserver and interobserver method on two separate occasions. The Chi statistic averaged over the 24 physicians was 59.6% (39.6— 79.6%).1 The Puusepp’s sign — a slow tonic abduction of the little toe in response to stroking the sole of the foot — was found to be a more reliable sign, being present in the absence of the Babinski sign. How-
R. Pauc ever, the results of this study were based on a very small population (6).22 The above results would stress the importance of not interpreting the Babinski sign in isolation but further that the test must be performed correctly and the examiner must have knowledge of the flexor reflex afferent response (an exaggerated flexor synergy response) in order to elicit the correct response and interpret it correctly.16,23,24 Electromyographical studies have been shown to be useful in recording responses from the effectors of this plantar response — flexor hallucis brevis, extensor hallucis longus and tibialis anterior (for the temporal relationship to the flexion reflex) when the plantar responses are equivocal.25 The Babinski sign has been reported as occurring following head trauma in children,26 after epileptic seizures,27 during nocturnal myoclonus,28 in children with learning and behavioural disorders,2 in patients without apparent corticospinal dysfunction,3 and in an elderly population where it might prove to be a marker of the onset of dementia along with certain other primitive reflexes.4
Discussion Babinski’s sign of the great toe, despite continuing controversy as to its function as a reliable indicator of corticospinal (pyramidal) dysfunction, remains one of the mainstays of the modern neurological examination and is described in established textbooks to this day. Classically the sign included the ‘‘signe de l’eventail’’ (fanning of the toes) and the ‘‘phenomenone des orteils’’ (the great toe sign). However, in 1903 Babinski himself stated that the fanning of the toes was not necessarily part of the reflex.10 Release of the flexion reflex synergy causing contraction of the extensor hallucis longus (innervated by the deep peroneal nerve) is the underlying cause of the manifestation that is the Babinski sign but is it always, particularly when unequivocal, pathological? In a prospective epidemiological study of 100 children attending a specialist clinic for the treatment of learning and behavioural disorders 46% were found to have an extensor plantar response.2 The response was predominantly unilateral on the right and often associated with a flexor reflex afferent response on the left. 47% of the children had previously been diagnosed as being dyslexic which is not generally considered to be a medical condition while the remainder had been diagnosed as suffering from attention deficit disorder (ADD), attention deficit hyperactivity disorder (ADHD), obsessive compulsive disorder (OCD), dyspraxia and Tourette’s
Babinski sign in sickness and health syndrome. In a study of 100 adult patients attending a medical centre with no history or clinical signs of pyramidal tract involvement, 10% had an extensor plantar response either unilaterally or bilaterally.3 Within 3 years of Babinski’s original publication research was under way for the sign occurring in normal healthy individuals. Schuler found the sign to be present in 6% of healthy men and women and Critchley noted that it was occasionally present in the elderly in the absence of any pyramidal tract involvement.29 Yakovlev and Farrell examined a group of soldiers before and after marching 14 miles and found the Babinski sign unilaterally in 7.2% and bilaterally in 1.2% following the march.30 Morgenthaler examined 200 schoolchildren taken from the playground and found extension of the big toe in 1.5% and fanning of the toes in 7.5%.30 Kaye found it to be present in 5.9% of a group aged 65—74 and at 12% in a group aged 85+ all of whom were in excellent health.31 It is therefore reasonable to question as to whether or not the Babinski response is always a sign of corticospinal involvement or at times a possible indicator of there being a retained primitive reflex suggestive of developmental delay in a child or a frontal release sign in the elderly. In a prospective epidemiological study of 100 children with learning and behavioural problems, 46% had a Babinski response and 42% had paratonia.2 The persistence of these primitive reflexes, a sign of uninhibited reflexive behaviour by descending pathways due to an under development and maturation of frontal brain areas, is perhaps borne out by the appearance of frontal release signs in an elderly population, notably associated with neuronal loss and the onset of dementia.31—33 The altered state or activity of neuronal fields and the loss of neurons in the anterior cingulate gyrus, fronto-insular cortex and dorsolateral prefrontal cortex have been implicated in the pathogenesis of autism, the learning and behavioural disorders of children, obsessive compulsive disorder, depression, anxiety, phobic states, psychopathy, anorexia, schizophrenia, fronto-temporal dementia and Alzheimer’s disease.34—37 The Babinski sign is a result of withdrawal of supraspinal control of flexor reflexes in the lower limb normally suppressed by the dorsal reticulospinal system arising from the pontomedullary reticular formation which descends in the dorsolateral funiculus of the spinal cord.7 It has been suggested that any alteration in the function of the corticoreticulospinal tract, which lies adjacent to the lateral corticospinal from cortex to spinal segment levels would cause the release of flexor reflexes.38 The corticospinal and corticobulbar tracts originates from motor fibers of the primary motor area,
125 premotor area, supplementary motor area and the anterior cingulate area. The first somesthetic area of the parietal cortex contributes some 40% of the fibers that constitute the corticospinal/bulbar tracts. A high percentage of the corticospinal/bulbar efferents terminate in the pontine and reticular nuclei of the pons and medullar.39 It has been suggested that neurons that are late to develop both in terms of phylogeny as well as ontogeny are particularly vulnerable to dysfunction.37 Of the neurons that fulfil that criteria, the von Economo neuron is potentially a candidate in the genesis of the Babinski response and paratonia — primitive reflexes/frontal release signs — as 85% develop in the postnatal period (4 months to 4 years) and are limited to just 3 locations in the human brain one of which is the anterior cingulate gyrus. The abnormal development, structure or functioning of von Economo neurons (VENs) of the anterior cingulate gyrus have been implicated in the pathogenesis of a range of neurodevelopmental, neuropsychiatric and neurodegenerative conditions that potentially can affect people of any age. Could it be that late development of these neuron fields due to stressors2,37 could cause abnormal functioning of the anterior cingulate gyrus that in turn alters the top down functioning of the corticospinal/bulbar tracts that release the flexor response in the absence of true corticospinal pathology?
Conclusion The Babinski sign has long been considered to be a classic sign of a corticospinal lesion and yet it has been found to be present in normal, healthy schoolchildren, in children suffering from learning and behavioural disorders, in young soldiers, in hospital patients without any signs of a corticospinal lesion and in healthy elderly people as well in an those suffering various types and degrees of dementia. Some 3 years after Babinski’s original work, the question was posed as to whether or not the Babinski sign could occur without involvement of the pyramidal tract and it would now appear that the answer is that it can. Various authors have noted the presence of the Babinski sign in the absence of corticospinal involvement by disease2,3,29—31 and others have pointed to a host of neurodevelopmental and neuropsychiatric disorders originating in the anterior cingulate gyrus.4,34—37,40 What we do know at present is that the anterior cingulate gyrus is intimately involved in the efferent pathway that forms the corticospinal tract. However, what we do not know at this present
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time is if and how it might be involved in the top down supraspinal control, possibly via the reticulospinal tract, of flexor reflexes in the lower limbs. Until such time as more advanced scanning techniques are available, we can only speculate as to whether or not the anterior cingulate and its VEN fields are in any way involved in the appearance of the Babinski sign in healthy children and adults. In the meantime it is reasonable to consider the Babinski sign as being evidence of a possible upper motor neuron lesion but also a sign of the state of development of the brain and notably the prefrontal cortex and its subsequent decline.
References 1. Maher J, Reilly M, Daly L, Hutchinson M. Plantar power: reproducibility of the plantar response. BMJ 1992;304:482. 2. Pauc R. Comorbidity of dyslexia, dyspraxia, attention deficit disorder (ADD), attention deficit hyperactive disorder (ADHD), obsessive compulsive disorder (OCD) and Tourette’s syndrome in children: a prospective epidemiological study. Clin Chiro 2005;8:189—98. 3. Filho P, Dib E, Ribeiro R. Babinski and Chaddock signs without apparent pyramidal dysfunction. Arq Neuro-Psiquiatr 2005; 63:484—7. 4. Damasceno A, Delicio A, Mazo D, Zullo J, Scherer P, Ng R, et al. Primitive reflexes and cognitive function. Arq NeuroPsiquiatr 2005;63(3):577—82. 5. Pearce J. Babinski or Remak? J R Coll Physicians Lond 1996;30:190. 6. Massey E, Sanders L. Babinski’s sign in medieval, Renaissance and baroque art. Arch Neurol 1989;46(January (1)):85—8. 7. Lance J. The Babinski sign. J Neurol Neurosurg Psychiatry 2002;73:360—2. 8. Babinski J. Sur le reflexe cutane plantaire dans certaines affections organiques du systeme nerveux central. C R Soc Biol 1896;48:207—8. 9. Babinski J. Du phenomene des orteils et de sa valeur semiologique. Sem Med 1898;18:321—2. 10. Babinski J. De l’abduction des orteils (signe de l’eventail). Rev Neurol (Paris) 1903;11:728—9. 11. Futagi Y, Suzuki Y. Neural mechanism and clinical significance of the plantar grasp reflex in infants. Pediatr Neurol 2010;43(2):81—6. 12. DeJong R. The neurologic examination. 5th ed. LippincootRaven; 1992. 13. Khwaja G. Plantar reflex. JIACM 2005;6(3):193—7. 14. Goetz C. History of the extensor plantar response: Babinski and Chaddock signs. Semin Neurol 2002;22(4):391—8. 15. Kumar S. The Babinski sign — a critical review. J Assoc Physicians India 2003;51:53—7. 16. Patten J. Neurological differential diagnosis. 2nd ed. Springer; 1996. 17. Babinski J. Hemispasme facial peripherique. Nouvelle iconographie de la Salpetriere 1905;18:418—23.
18. Van Gijn J, Bonke B. Interpretation of plantar reflexes: biasing effect of other signs and symptoms. J Neurol Neurosurg Psychiatry 1977;40:787—9. 19. Singerman J, Lee L. Consistency of the Babinski reflex and its variants. Eur J Neurol 2008;15(9):960—4. 20. Miller T, Johnson S. Should the Babinski sign be part of the routine neurologic examination? Neurology 2005;25(65 (8)):1165—8. 21. McCrance C, Watt J, Hall D. An evaluation of the reliability and validity of the plantar response in a psychogeriatric population. J Chronic Dis 1968;21:369—74. 22. Tacik P, Krasnianski M, Zierz S. Puusepp’s sign — clinical significance of a forgotten pyramidal sign. Clin Neurol Neurosurg 2009;111(December):919—21. 23. Raijmakers P, Cabezas M, Smal J, Van Gijn J. Teaching the plantar reflex. Clin Neurol Neurosurg 1991;93(3):201—4. 24. Glick T. Towards a more efficient and effective neurologic examination for the 21st century. Eur J Neurol 2005;12(12): 994—7. 25. Van Gijn J. Equivocal plantar responses: a clinical and electromyographic study. J Neurol Neurosurg Psychiatry 1976;39:275—82. 26. Parish R, Woolf A, Eichner M, Cauldwell C. The significance of Babinski signs in children with head trauma. Ann Emerg Med 1985;14(4):329—30. 27. Walczak T, Rubinsky M. Plantar responses after epileptic seizures. Neurology 1994;44(11):2191—3. 28. Smith R. Relationship of periodic movements in sleep (nocturnal myoclonus) and the Babinski sign. Sleep 1985;8(3):239—43. 29. Van Gijn J. The Babinski sign: a centenary. Utrecht, Heidelberglaan, Netherlands: University Utrecht; 1996. 30. Nathan P, Smith M. The Babinski response: a review and new observations. J Neurol Neurosurg Psychiatry 1955;18:250—9. 31. Kaye J, Oken B, Howieson J, Holm L, Dennison K. Neurologic evaluation of the optimally healthy oldest old. Arch Neurol 1994;51(12):1205—11. 32. Pauc R, Young A. Paratonia and gegenhalten in childhood and senescence. Clin Chiropr 2010; doi: 10.1016/j.clch.2011. 08.001. 33. Hogan D, Ebly E. Primitive reflexes and dementia: results from the Canadian study of health and ageing. Age Ageing 1995;24:375—81. 34. Nimchinsky E, Vogt B, Morrison J, Hof P. Spindle cells of the human anterior cingulate cortex. J Comp Neurol 1995;355: 27—37. 35. Seeley W, Carlin D, Allman J, Macedo N, Bush C, Miller B, et al. Early frontotemporal dementia targets neurons unique to apes and humans. Ann Neurol 2006;60:660—7. 36. Allman J, Hakeem A, Erwin J, Hof P. The anterior cingulate cortex — the evolution of an interface between emotion and cognition. Ann NY Acad Sci 2001;935:107—17. 37. Allman J, Watson K, Tetreault N, Hakeem A. Intuition and autism: a possible role for von Economo neurons. Trends Cognit Sci 2005;9:367—73. 38. Lance J. The control of muscle tone, reflexes and movement. Robert Wartenberg lecture. Neurology 1980;30:1303—13. 39. Kiernan J. Barr’s the human nervous system. 9th ed. Wolters Kluwer Lippincott Williams Wilkins; 2008. 40. Pauc R, Young A. Little known neurons of the medial wall: a literature review of pyramidal cells of the cingulate gyrus. J Chiro Med 2010;9:115—20.
Available online at www.sciencedirect.com
www.elsevier.com/locate/clch
LITERATURE REVIEW
The Babinski sign in sickness and in health Robin Pauc * The Tinsley House Clinic, Main Road, East Boldre, Hants, UK Received 16 September 2010; received in revised form 25 June 2011; accepted 6 July 2011
KEYWORDS Babinski; Babinski sign; Extensor plantar response; Neurological examination; Superficial abdominal reflex
Summary The Babinski sign is a well documented phenomenon and testing for its presence forms part of the standard neurological examination. However, although historically it is considered to indicate an upper motor neuron lesion related to pathology anywhere in the course of the corticospinal tract, it has been found to be present in healthy children, in adults, and in increasing numbers in the elderly population. It may therefore also be a sign of the state of development of the brain and its subsequent decline. Objective: To draw together research being conducted into the Babinski sign, how it should be performed, how it should be evaluated, its validity and possible falsepositive extensor plantar responses seen as a result of developmental delay in both children and adults. Design: This study was a review of the available literature retrieved from computerised databases, the world wide web and authoritative texts. Method: All the information on current and past research was gathered from a computerised literature search of MEDLINE, Science Direct, Cochrane Library, Science Citation Index, SCOPUS, CINAHL and the world wide web. The search terms used were Babinski, Babinski sign, extensor plantar response. # 2011 The College of Chiropractors. Published by Elsevier Ltd. All rights reserved.
Contents Introduction . . . . . . . . . . . . . . . . . . History . . . . . . . . . . . . . . . . . . . . . . Normal reflexive development . . . . The Babinski sign . . . . . . . . . . . . . . Evaluation of results and validity of Discussion . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . .
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* Fax: +44 01590 612432. E-mail address: [email protected]. 1479-2354/$36.00 # 2011 The College of Chiropractors. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.clch.2011.07.007
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123 123 123 123 124 124 125 126
Babinski sign in sickness and health
Introduction The Babinski sign is well known to both students and practitioners alike and testing for its presence forms part of the standard neurological examination performed on virtually every patient and yet over the years its validity has been questioned and to date no one has satisfactorily explained what are the necessary neurodevelopmental changes that must take place before the primitive response seen in infants is replaced by the adult form.1 It has been found to be present in a high percentage of children diagnosed as suffering from learning and behavioural disorders and in a number of patients otherwise lacking signs of corticospinal damage.2,3 It returns in a number of otherwise healthy elderly subjects and may therefore indicate a decline in mental function associated with age related neuronal loss and the onset of dementia.4
History Although the discovery of the sign is attributed to Joseph Felix Francois Babinski, it had previously been described by Robert Remak (1815—1867) and had been portrayed in medieval, Renaissance and baroque art as occurring in infants.5,6 Remak first described the extensor plantar response in 1893 describing the response he had noted in a patient with transverse myelitis as follows: ‘‘One is able, through stroking the distal half of the plantar aspect of the metatarsus primus, to evoke a fairly isolated reflex of the extensor hallucis longus’’.7 In 1896 Babinski published a preliminary report of just 28 lines on the ‘‘reflexe cutane plantaire’’ (cutaneous plantar reflex) in which he described the phenomenon of the toes — signe de l’eventail — an extension of all toes with noxious stimulation (pricking) of the sole of the foot.8 It was not until 1898 that he specifically described the extension of the hallux with strong tactile stimulation (stroking) of the lateral border of the sole.9 In a third paper published in 1903 Babinski stated that if others had described the abnormal reflex before him they had found it fortuitously and did not realise its semiologic value.10
Normal reflexive development The plantar grasp reflex, a rudimentary response essential to infant apes in arboreal life, is considered to be one of the most primitive of the primitive reflexes and can be elicited in all pre-
123 term infants from 25 weeks of postconceptional age and continues to be present until 6 months postnatally. It is elicited by applying pressure to the sole of the foot just behind the toes. The infant should be placed in the supine position, must be awake and have the head in the midline position to avoid evoking an asymmetric tonic neck reflex. It is tonic in character and persists for 15—30 s following initiation.11 The plantar reflex is obtained by stroking the lateral aspect of the plantar surface of the foot from the heel towards the toes and then across the foot towards the medial aspect avoiding the flexor tendons and the ball of the great toe. The usual dominant response is that of plantar flexion of the toes and foot. The reflex is innervated by the tibial nerve (fourth lumbar through first or second sacral segment). This superficial reflex should be established by 12—18 months replacing the more primitive reflexive response of an extensor plantar seen in infants before this age.12 The timing of the change from the infantile to adult response has been related to the onset of walking.13
The Babinski sign The testing of the plantar reflex is a pivotal part of the standard neurological examination and the Babinski sign or response has been considered for many years to be the sine qua non among the pathological reflexes indicative of corticospinal tract lesions of the cortex, subcortex, brainstem or spinal cord.14 The sign itself consists of dorsiflexion of the big toe by recruitment of the extensor hallucis longus muscle following stimulation of the lateral aspect of the sole of the foot with a blunt object. Babinski himself noted the relationship between this sign and the shortening of other leg musculature as part of the flexion synergy of the lower limb.15 Care must be taken when testing the plantar reflex not to cause frank pain which may elicit a defensive withdrawal response which may be confused with a flexor reflex afferent response often found with a unilateral Babinski sign.16 Historically, the Babinski sign was the failure of the platysma muscle to contract on the side of a hemiparesis as described by Babinski in 1905.17 However, with time the eponym for the ‘‘great toe sign’’ of Babinski has stuck and is now firmly established as the name applied to dorsiflexion of the great toe with or without fanning of the other toes and withdrawal of the leg on plantar stimulation in patients with lesions of the corticospinal tract.
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Evaluation of results and validity of the Babinski sign In an ideal world the examination process should confirm the diagnostic impression and the Babinski sign would be present or absent. However, the Babinski response can be equivocal and information gleaned from the consultation and examination may bias an equivocal response towards being Babinski positive or absent.18 In a study of thity-four patients the inter- and intra-observer consistency of the Babinski reflex and its variants — Gordan, Chaddock and Oppenheim reflexes — were assessed following the examination of the patients by six neurologists. The Babinski reflex had the highest interobserver consistency with a kappa value of 0.491, while the Chaddock, Oppenheim and Gordon reflexes had kappa values of 0.4065, 0.3739 and 0.3515, respectively. The Babinski and Chaddock signs together have been found to be the most reliable tests for the lower limbs. The authors concluded that the Babinski reflex was the most consistent reflex between examiners but that the small sample size limited the conclusions that could be drawn from their results.19 In a second study the validity of the Babinski reflex was assessed again using the interobserver method (five neurologists and five non-specialists) and it was found that the reliability and validity of the Babinski reflex was fair with a kappa value of 0.30 but that foot tapping was substantially more reliable with a kappa value of 0.73. Again, the small sample size of just ten subjects must be taken into consideration as with the previous interobserver study.20 An evaluation of the reliability and validity of the Babinski reflex in a psychogeriatric population found that the response sets did not occur at random (P < 0.001) but that the reproducibility was so low that its clinical value in this elderly population was seriously questioned.21 This is somewhat surprising as in other studies it has been found to occur with greater frequency in both a healthy elderly adult population and in association with the onset of dementia.4 The reproducibility of the Babinski sign was assessed using 24 physicians and 12 patients again by means of the intraobserver and interobserver method on two separate occasions. The Chi statistic averaged over the 24 physicians was 59.6% (39.6— 79.6%).1 The Puusepp’s sign — a slow tonic abduction of the little toe in response to stroking the sole of the foot — was found to be a more reliable sign, being present in the absence of the Babinski sign. How-
R. Pauc ever, the results of this study were based on a very small population (6).22 The above results would stress the importance of not interpreting the Babinski sign in isolation but further that the test must be performed correctly and the examiner must have knowledge of the flexor reflex afferent response (an exaggerated flexor synergy response) in order to elicit the correct response and interpret it correctly.16,23,24 Electromyographical studies have been shown to be useful in recording responses from the effectors of this plantar response — flexor hallucis brevis, extensor hallucis longus and tibialis anterior (for the temporal relationship to the flexion reflex) when the plantar responses are equivocal.25 The Babinski sign has been reported as occurring following head trauma in children,26 after epileptic seizures,27 during nocturnal myoclonus,28 in children with learning and behavioural disorders,2 in patients without apparent corticospinal dysfunction,3 and in an elderly population where it might prove to be a marker of the onset of dementia along with certain other primitive reflexes.4
Discussion Babinski’s sign of the great toe, despite continuing controversy as to its function as a reliable indicator of corticospinal (pyramidal) dysfunction, remains one of the mainstays of the modern neurological examination and is described in established textbooks to this day. Classically the sign included the ‘‘signe de l’eventail’’ (fanning of the toes) and the ‘‘phenomenone des orteils’’ (the great toe sign). However, in 1903 Babinski himself stated that the fanning of the toes was not necessarily part of the reflex.10 Release of the flexion reflex synergy causing contraction of the extensor hallucis longus (innervated by the deep peroneal nerve) is the underlying cause of the manifestation that is the Babinski sign but is it always, particularly when unequivocal, pathological? In a prospective epidemiological study of 100 children attending a specialist clinic for the treatment of learning and behavioural disorders 46% were found to have an extensor plantar response.2 The response was predominantly unilateral on the right and often associated with a flexor reflex afferent response on the left. 47% of the children had previously been diagnosed as being dyslexic which is not generally considered to be a medical condition while the remainder had been diagnosed as suffering from attention deficit disorder (ADD), attention deficit hyperactivity disorder (ADHD), obsessive compulsive disorder (OCD), dyspraxia and Tourette’s
Babinski sign in sickness and health syndrome. In a study of 100 adult patients attending a medical centre with no history or clinical signs of pyramidal tract involvement, 10% had an extensor plantar response either unilaterally or bilaterally.3 Within 3 years of Babinski’s original publication research was under way for the sign occurring in normal healthy individuals. Schuler found the sign to be present in 6% of healthy men and women and Critchley noted that it was occasionally present in the elderly in the absence of any pyramidal tract involvement.29 Yakovlev and Farrell examined a group of soldiers before and after marching 14 miles and found the Babinski sign unilaterally in 7.2% and bilaterally in 1.2% following the march.30 Morgenthaler examined 200 schoolchildren taken from the playground and found extension of the big toe in 1.5% and fanning of the toes in 7.5%.30 Kaye found it to be present in 5.9% of a group aged 65—74 and at 12% in a group aged 85+ all of whom were in excellent health.31 It is therefore reasonable to question as to whether or not the Babinski response is always a sign of corticospinal involvement or at times a possible indicator of there being a retained primitive reflex suggestive of developmental delay in a child or a frontal release sign in the elderly. In a prospective epidemiological study of 100 children with learning and behavioural problems, 46% had a Babinski response and 42% had paratonia.2 The persistence of these primitive reflexes, a sign of uninhibited reflexive behaviour by descending pathways due to an under development and maturation of frontal brain areas, is perhaps borne out by the appearance of frontal release signs in an elderly population, notably associated with neuronal loss and the onset of dementia.31—33 The altered state or activity of neuronal fields and the loss of neurons in the anterior cingulate gyrus, fronto-insular cortex and dorsolateral prefrontal cortex have been implicated in the pathogenesis of autism, the learning and behavioural disorders of children, obsessive compulsive disorder, depression, anxiety, phobic states, psychopathy, anorexia, schizophrenia, fronto-temporal dementia and Alzheimer’s disease.34—37 The Babinski sign is a result of withdrawal of supraspinal control of flexor reflexes in the lower limb normally suppressed by the dorsal reticulospinal system arising from the pontomedullary reticular formation which descends in the dorsolateral funiculus of the spinal cord.7 It has been suggested that any alteration in the function of the corticoreticulospinal tract, which lies adjacent to the lateral corticospinal from cortex to spinal segment levels would cause the release of flexor reflexes.38 The corticospinal and corticobulbar tracts originates from motor fibers of the primary motor area,
125 premotor area, supplementary motor area and the anterior cingulate area. The first somesthetic area of the parietal cortex contributes some 40% of the fibers that constitute the corticospinal/bulbar tracts. A high percentage of the corticospinal/bulbar efferents terminate in the pontine and reticular nuclei of the pons and medullar.39 It has been suggested that neurons that are late to develop both in terms of phylogeny as well as ontogeny are particularly vulnerable to dysfunction.37 Of the neurons that fulfil that criteria, the von Economo neuron is potentially a candidate in the genesis of the Babinski response and paratonia — primitive reflexes/frontal release signs — as 85% develop in the postnatal period (4 months to 4 years) and are limited to just 3 locations in the human brain one of which is the anterior cingulate gyrus. The abnormal development, structure or functioning of von Economo neurons (VENs) of the anterior cingulate gyrus have been implicated in the pathogenesis of a range of neurodevelopmental, neuropsychiatric and neurodegenerative conditions that potentially can affect people of any age. Could it be that late development of these neuron fields due to stressors2,37 could cause abnormal functioning of the anterior cingulate gyrus that in turn alters the top down functioning of the corticospinal/bulbar tracts that release the flexor response in the absence of true corticospinal pathology?
Conclusion The Babinski sign has long been considered to be a classic sign of a corticospinal lesion and yet it has been found to be present in normal, healthy schoolchildren, in children suffering from learning and behavioural disorders, in young soldiers, in hospital patients without any signs of a corticospinal lesion and in healthy elderly people as well in an those suffering various types and degrees of dementia. Some 3 years after Babinski’s original work, the question was posed as to whether or not the Babinski sign could occur without involvement of the pyramidal tract and it would now appear that the answer is that it can. Various authors have noted the presence of the Babinski sign in the absence of corticospinal involvement by disease2,3,29—31 and others have pointed to a host of neurodevelopmental and neuropsychiatric disorders originating in the anterior cingulate gyrus.4,34—37,40 What we do know at present is that the anterior cingulate gyrus is intimately involved in the efferent pathway that forms the corticospinal tract. However, what we do not know at this present
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time is if and how it might be involved in the top down supraspinal control, possibly via the reticulospinal tract, of flexor reflexes in the lower limbs. Until such time as more advanced scanning techniques are available, we can only speculate as to whether or not the anterior cingulate and its VEN fields are in any way involved in the appearance of the Babinski sign in healthy children and adults. In the meantime it is reasonable to consider the Babinski sign as being evidence of a possible upper motor neuron lesion but also a sign of the state of development of the brain and notably the prefrontal cortex and its subsequent decline.
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