Case Rep Neurol

DOI: 10.1159/000474935 2017 The Author(s)

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Case Report

The Crossed Flexor Plantar Response

in Patients with Klippel-Feil
Syndrome
Anna Sadnicka Simon F. Farmer
The National Hospital for Neurology and Neurosurgery, London, UK

Keywords
Klippel-Feil syndrome Flexor plantar response Plantar reflex Mirror movements

Abstract
The plantar reflex is one of most important and widely tested components of the neurologi-
cal examination. We describe 3 subjects with Klippel-Feil syndrome and mirror movements
where unilateral cutaneous stimulation of the foot leads to flexor plantar responses in both
feet. We discuss the evidence which suggests that this crossed flexor plantar response re-
veals a transcortical pathway for the flexor plantar response. 2017 The Author(s)
Published by S. Karger AG, Basel

Background

Klippel-Feil syndrome is a rare skeletal anomaly characterised by abnormal fusion of

two or more vertebrae and the clinical triad of a short neck with restricted movement and a
low posterior hairline (Fig. 1a) [1, 2]. Sporadic and genetic forms (autosomal dominant, re-
cessive, and x-linked) are described and the syndrome is most commonly diagnosed prena-
tally or at birth [3].
Klippel-Feil syndrome is associated with mirror movements by which voluntary unilat-
eral movement of a limb causes involuntary movement or mirroring of the homologous mus-
cles of the opposite limb [4, 5]. Mirror movements are most often observed in the hands but
can also be seen in distal lower limb musculature [6]. Magnetic resonance imaging (MRI) of

Dr. Simon F. Farmer

The National Hospital for Neurology and Neurosurgery
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Queen Square
London WC1N 3BG (UK)
E-Mail [Link]@[Link]
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 Case Rep Neurol 122
DOI: 10.1159/000474935 2017 The Author(s). Published by S. Karger AG, Basel
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Sadnicka and Farmer: The Crossed Flexor Plantar Response in Patients with Klippel-Feil
Syndrome

the cervicomedullary junction of such patients demonstrates varying degrees of neuroschisis

(posterior cleft through to complete neuroschisis), and increasing neuroschisis is associated
with more prominent mirror movements [6] (Fig. 1b).
In this paper, we describe a novel physical sign seen in patients with Klippel-Feil syn-
drome who have mirror movements: the crossed flexor plantar response. In 3 patients, uni-
lateral mechanical stimulation of the foot produced bilateral flexor plantar responses. We
discuss how this novel clinical sign may shed further light on the anatomical pathway of the
flexor plantar response in health.

Case Presentation

Three female patients (aged 39, 45, and 45 years) with Klippel-Feil syndrome were seen
at the National Hospital for Neurology and Neurosurgery and St Marys Hospital, London,
UK. Written informed consent was obtained from the patients for the images and videos to
be published. All patients had mirror movements of the fingers and toes. For example, 1 pa-
tient reported that when practising the piano if rehearsing 1 hand she would sit on the other
hand to stop mirror movements from occurring. On examination, deep tendon reflexes were
present and not crossed. During plantar response, testing subjects were asked to relax and
to avoid voluntary movement during testing. Both right and left feet were stimulated at dif-
ferent times and the bilateral flexor plantar response sign was seen in all 3 subjects regard-
less of whether the right or left foot was stimulated. This is exemplified in a series of photo
stills (Fig. 2) and in the online supplementary Video (see
[Link]/doi/10.1159/000474935).

Discussion

The plantar response is a critical component of the neurological examination. The epon-
ymous positive Babinski sign signifies disturbance of the pyramidal tract by upward move-
ment of the great toe [7]. Implicit in our understanding is a belief that in order to produce a
healthy flexor plantar response, the intact central nervous pathways exert control over a
more primitive extensor plantar. This is supported by the observation that children, before
they become ambulant, exhibit an extensor plantar response that is then corticalised by
maturation of central motor pathways. Whilst these models of motor physiology make intui-
tive sense, they do not tell us with precision the pathways implicated in the plantar re-
sponse, and whether the plantar reflex is solely spinal or transcortical has been the subject
of much debate [8]. We discuss evidence that the crossed flexor plantar response in Klippel-
Feil syndrome with mirror movements may shed further light on the neuroanatomy of the
plantar reflex pathway.
In healthy individuals, transcranial magnetic or electrical stimulation of the motor cor-
tex typically elicits muscle contraction in the opposite side of the body only. In patients with
Klippel-Feil syndrome and mirror movements, stimulation to either hemisphere evokes bi-
lateral simultaneous responses [9]. The short latency of the unilateral and contralateral mo-
tor evoked responses (approximately 20 ms) is fully compatible with corticospinal conduc-
tion, and the ipsilateral responses are thought to be mediated by an anomalous uncrossed
corticospinal pathway [9]. Furthermore, when electromyography (EMG) is used to study
mirror movements, cross-correlation analysis of the simultaneous left and right muscle ac-
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 Case Rep Neurol 123
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Sadnicka and Farmer: The Crossed Flexor Plantar Response in Patients with Klippel-Feil
Syndrome

tivity reveals that there is short-term motor unit synchrony between homologous muscle
pairs [9]. This is not observed in non-mirroring subjects and is indicative of abnormal com-
mon monosynaptic input to the left and right motor neurone pools in Klippel-Feil syndrome
[9]. The hypothesis of aberrant corticospinal tracts is further supported by abnormalities of
pyramidal decussation found on the autopsy of a person with Klippel-Feil syndrome [10].
These abnormal anatomical features in Klippel-Feil syndrome have therefore been used
as a model by which to probe the neuroanatomical basis of motor phenomena observed in
healthy subjects. For example, in Klippel-Feil syndrome during unilateral stimulation of
stretch and cutaneous afferent pathways, there is crossing of the long-latency stretch and
long-latency cutaneomuscular reflexes without crossing of short-latency components of the
reflexes [9, 11]. As the bilateral long-latency responses are remarkably symmetrical in their
temporal and amplitude characteristics with a similar muscle distribution and behaviour,
these neurophysiological observations revealed that these later components of the reflex are
transcortical [9, 11]. Our observation detailing an abnormally crossed flexor plantar re-
sponse in 3 patients therefore provides strong evidence that their plantar response is also
mediated by a transcortical reflex. To date, there is no evidence of an abnormally organised
somatosensory pathway [9] in these patients.
Generalisation of our interpretation of this result to the flexor plantar response ob-
served in neurologically intact adult subjects without mirror movements is difficult given
that the Klippel-Feil syndrome subjects have highly abnormal neuro-anatomy at the brain-
stem and cervical levels. However, the plantar responses we observed are qualitatively the
same as those seen in normal subjects. Furthermore, our findings fit well with what is known
about the plantar response, i.e., that it becomes flexor during motor development as spinal
reflex pathways become subject to cortical control and that damage to the motor cortex
and/or the descending white matter tracts leads to release of the reflex the extensor
plantar response or Babinski sign.
It is unusual to be able to describe a new physical sign, albeit in an unusual yet informa-
tive group of patients. Careful consideration of the nature of the crossed plantar reflex in
patients with Klippel-Feil syndrome and mirror movements may be used to inform our un-
derstanding of the mechanisms that underlie one of the commonest and most important
parts of the neurological examination, the flexor plantar reflex.

Acknowledgements

We would like to thank the patients included in this study. We thank Dr. Jonathon
Frankel for referring one of the cases and Dr. John Stevens for reviewing the radiology.

Statement of Ethics

Written informed consent was obtained from the patients for the images and videos to
be published.
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 Case Rep Neurol 124
DOI: 10.1159/000474935 2017 The Author(s). Published by S. Karger AG, Basel
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Sadnicka and Farmer: The Crossed Flexor Plantar Response in Patients with Klippel-Feil
Syndrome

Disclosure Statement

On behalf of all authors, the corresponding author states that there are no conflicts of in-
terest.

References

1 Noble TP, Frawley JM: The Klippel-Feil syndrome: numerical reduction of cervical vertebrae. Ann Surg
1925;82:728734.
2 Saker E, Loukas M, Oskouian RJ, Tubbs RS: The intriguing history of vertebral fusion anomalies: the
Klippel-Feil syndrome. Childs Nerv Syst 2016;32:15991602.
3 Giampietro PF, Raggio CL, Blank RD, McCarty C, Broeckel U, Pickart MA: Clinical, genetic and
environmental factors associated with congenital vertebral malformations. Mol Syndromol 2013;4:94
105.
4 Bauman GI: Absence of the cervical spine: Klippel-Feil syndrome. J Am Med Assoc 1932;98:129132.
5 Baird PA, Robinson GC, Buckler WS: Klippel-Feil syndrome. A study of mirror movement detected by
electromyography. Am J Dis Child 1967;113:546551.
6 Royal SA, Tubbs RS, DAntonio MG, Rauzzino MJ, Oakes WJ: Investigations into the association between
cervicomedullary neuroschisis and mirror movements in patients with Klippel-Feil syndrome. AJNR
Am J Neuroradiol 2002;23:724729.
7 Babiski JJFF: Sur le rflexe cutan plantaire dans certaines affections organiques du systme nerveux
central. C R Seanc Soc Biol 1896;3:207208.
8 Landau WM, Clare MH: The plantar reflex in man, with special reference to some conditions where the
extensor response is unexpectedly absent. Brain 1959;82:321355.
9 Farmer SF, Ingram DA, Stephens JA: Mirror movements studied in a patient with Klippel-Feil syndrome.
J Physiol 1990;428:467484.
10 Gunderson C, Solitare G: Mirror movements in patients with the Klippel-Feil syndrome.
Neuropathological observations. Arch Neurol 1968;18:675679.
11 Matthews PB, Farmer SF, Ingram DA: On the localization of the stretch reflex of intrinsic hand muscles
in a patient with mirror movements. J Physiol 1990;428:561577.

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Sadnicka and Farmer: The Crossed Flexor Plantar Response in Patients with Klippel-Feil
Syndrome

Fig. 1. a The clinical triad of Klippel-Feil syndrome; a short neck, low hairline, and limited neck mobility.
b Axial MRI image at the level of the medullary pyramids shows typical cervicomedullary neuroschisis. In
this subject, the cleft extended caudally to the levels at which the cervical roots emerged.
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Sadnicka and Farmer: The Crossed Flexor Plantar Response in Patients with Klippel-Feil
Syndrome

Fig. 2. The crossed flexor plantar response. Stills from the online supplementary Video show flexion in both
toes after sensory stimulation to the right foot only.

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