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CASE REPORT

Ipsilateral Motor Innervation Discovered


Incidentally on Intraoperative Monitoring:
A Case Report
Jerry Ku, MD∗ BACKGROUND AND IMPORTANCE: Lesions in the corticospinal tract above the decus-
Daniel Mendelsohn, MD∗ sation at the medullary pyramids almost universally produce contralateral deficits. Rare
Jason Chew, MB, ChB‡ cases of supratentorial lesions causing ipsilateral motor deficits have been reported
Jason Shewchuk, MD‡ previously, but only ever found secondary to stroke or congenital pyramidal tract
malformations.
Charles Dong, PhD∗
CLINICAL PRESENTATION: Herein, we report a case of ipsilateral corticospinal tract
Ryojo Akagami, MD∗ innervation discovered incidentally with intraoperative monitoring during a microsur-

Division of Neurosurgery, Department
gical resection of a vestibular schwannoma. Intraoperative monitoring with electrical
of Surgery, Faculty of Medicine, Univer- transcranial stimulation of the frontal scalp triggered motor-evoked potentials in the
sity of British Columbia, Vancouver, ipsilateral arms. The uncrossed pathways were later confirmed with MRI tractography using
British Columbia, Canada; ‡ Division of
Neuroradiology, Department of Radi-
diffusion tensor imaging.
ology, Faculty of Medicine, University CONCLUSION: To the best of our knowledge, this is the first case of isolated ipsilateral
of British Columbia, Vancouver, British motor innervation of the corticospinal tract discovered incidentally during a neurosur-
Columbia, Canada
gical procedure. Given the increasing use of intraoperative monitoring, this case under-
Correspondence: scores the importance of cautious interpretation of seemingly discordant neurophysio-
Ryojo Akagami, MD. logical findings. Once technical issues have been ruled out, ipsilateral motor innervation
Gordon and Leslie Diamond Health may be considered as a possible explanation and neurosurgeons should be aware of the
Care Centre,
8109 – 2775 Laurel Street, existence of this rare anatomic variant.
Vancouver, BC V5Z 1M9, Canada.
KEY WORDS: Ipsilateral motor innervation, Corticospinal tract, Intraoperative monitoring, Diffusion-weighted
E-mail: ryojo.akagami@vch.ca
imaging, Tractography
Received, November 18, 2015.
Neurosurgery 80:E194–E200, 2017 DOI:10.1093/neuros/nyw074 www.neurosurgery-online.com
Accepted, November 11, 2016.
Published Online, January 10, 2017.

Copyright 
C 2016 by the BACKGROUND AND IMPORTANCE ative monitoring are discussed within the context
Congress of Neurological Surgeons of this unusual nervous system variant.
Although a variable proportion of fibers cross
within the corticospinal tracts in humans,1
lesions rostral to the medullary pyramids CLINICAL PRESENTATION
almost universally cause contralateral extremity A 28-year-old right-handed Caucasian female
weakness. Rare cases of supratentorial lesions presented with progressive right ear hearing loss,
causing ipsilateral motor deficits have been numbness of the chin, cheek and tongue, right
reported previously, but only ever found eye tearing, and imbalance developing over 6
secondary to stroke2-5 or congenital pyramidal months. There was no facial motor asymmetry at
tract malformations.4,6,7 baseline. The patient was previously healthy with
We report a case of ipsilateral corticospinal an unremarkable family history. Physical exami-
tract innervation discovered incidentally with nation revealed horizontal end-gaze nystagmus,
intraoperative monitoring during a microsur- decreased right V2 and V3 sensation, and dimin-
gical resection of a vestibular schwannoma. ished right-sided corneal and gag reflexes. An
The uncrossed pathways were confirmed with audiogram showed right unilateral sensorineural
diffusion tensor imaging (DTI). The anatomy hearing loss. A brain MRI demonstrated a 3.0 ×
of the corticospinal tracts, neurobiology of 2.4 × 3.0 cm right-sided intracanalicular internal
fiber crossing, methods for investigating human auditory canal and cerebellopontine angle mass,
motor pathways, and implications in intraoper- displacing the trigeminal nerve superiorly and

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IPSILATERAL MOTOR INNERVATION

stimulation was applied with spiral needle electrodes at C3 or


C4 (anode) and Cz (cathode). Each pulse train consisted of 3
electrical pulses of 100 μs in width and 150 to 160 V in intensity
with an interstimulus interval (ISI) of 1 μs. Facial MEPs were
produced with TcES applied at an electrode on the left frontal
scalp (C3) referenced to Cz and recorded from the right orbic-
ularis oris (Figure 2C). Stimuli consisted of trains of 6 pulses of
100 μs in width and 160 V with an ISI of 1 μs. Left facial MEPs
were not assessed.
While obtaining baseline tracings, electrical transcranial stimu-
lation of the frontal scalp triggered MEPs in the ipsilateral
arms. After comprehensive troubleshooting and verification of
proper monitoring techniques, a technical etiology was excluded.
Functionally uncrossed corticospinal tracts were the presumed
cause, and the case proceeded without incident. Of note, the
SSEPs were appropriately contralaterally innervated. A gross total
resection was achieved with no intraoperative or postoperative
complications.

Postoperative Course
The patient reported marked improvement in unsteadiness
postoperatively. Audiograms indicated residual hearing in the
FIGURE 1. Preoperative axial fat-saturated T1-weighted MRI post-
gadolinium administration. A 3.0 × 2.4 × 3.0 cm mass is visualized in the right ear. Her facial function remained normal. There was still
right internal auditory canal (white arrow) and cerebellopontine angle (black mild nystagmus on right lateral gaze. An immediate postoperative
arrow), consistent with a vestibular schwannoma. MRI including DTI demonstrated resection of the right acoustic
neuroma with findings consistent with postoperative granulation
tissue (Figure 3). A delayed follow-up MRI with repeat DTI was
also obtained 2 years later, once the parenchymal distortion and
extending inferiorly past the jugular foramen (Figure 1). Mild postsurgical changes had resolved (Figure 4). MRI scans were
distortion of the pons was noted. The clinical picture and performed on a Siemens Aera 1.5T scanner with a 20-channel
imaging were consistent with a right vestibular schwannoma. receive-only head coil (Siemens, Munich, Germany). Standard
Informed consent was received from the patient for a retrosigmoid DTI using 20 diffusion directions and 5 mm slices was performed
craniotomy for microsurgical resection. of the whole head including the skull base. Postprocessing was
performed using the SyngoVia thin-client (Siemens) at a picture
Operative Procedure archiving and communication system workstation by a neurora-
After left lateral decubitus positioning, neurophysio- diologist. Both immediate postoperative and delayed follow-up
logical intraoperative monitoring of median and tibial nerve scans confirmed the uncrossed corticospinal tracts on DTI. No
somatosensory evoked potential (SSEP) and facial and further brain anatomic abnormalities were present.
upper limb motor evoked potential (MEP) were established
(Figure 2). With stimulation of the median nerve at the wrist and DISCUSSION
the tibial nerve at the ankle, SSEP responses were registered in the
peripheral and cortical channels. Stimuli consisted of repetitive Intraoperative monitoring is increasingly used to monitor
rectangle electrical pulses with the pulse width of 200 μs and nervous tissue function during brain and spine surgery when
intensity of 25 mA for the median nerve and 50 mA for the tibial eloquent structures are at risk.8-10 Extremity and facial MEPs are
nerve, delivered at 4.7 Hz. Cortical SSEP responses were recorded highly sensitive to detect corticospinal and corticobulbar injury
with scalp electrodes at CPc (active)/CPi (reference) following during surgery.8-10 When monitoring abnormalities occur, the
activation of the median nerve and at CPz (active)/FPz (reference) surgical team must determine if they are related to events at
and CPz (active) /CPc (reference) following stimulation of the the surgical site or due to confounding factors. Gradual gener-
tibial nerve. Peripheral SSEP responses were recorded at the alized MEP reductions suggest systemic factors such as anesthesia
medial surface of the arm 2 and 5 cm above the cubital crease depth or fade, whereas more abrupt generalized reduction may be
(Brp and Brd, respectively). MEPs were elicited with transcranial seen with stimulus failure, sedation boluses, abrupt hypotension,
electrical stimulation (TcES) and obtained from the bilateral neuromuscular blockade, or bilateral intracranial air.11 Focal
first dorsal interosseous and flexor carpi ulnaris (Figure 2B). MEP deterioration is the hallmark of surgical neurological
MEPs from the lower extremities were not assessed. Pulse train injury, but can also be due to confounding factors such as

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KU ET AL

FIGURE 2. A, Illustration of scalp electrodes placed for eliciting MEP and SSEP. Letters and numbers are according to the International 10–20 System of Electrode
Placement. B, Stimulation of the left motor cortex (C3/Cz) showed MEPs in the left first dorsal interosseous (DI) and flexor carpi ulnaris (FCU), and stimulation of
the right motor cortex (C4/Cz) showed MEPs in the right first DI and FCU, with no activity on the contralateral side. C, Stimulation of the left frontal scalp produced
right facial MEP and left first DI MEP.

downward electrode displacement, brachial plexus, or peripheral Only a few cases of clinically ipsilateral innervation of the corti-
nerve conduction failure due to limb malpositioning, pressure cospinal tract have been reported in the literature. 3-5,12-21 These
or ischemia, or asymmetric intracranial air.11 Seemingly spurious patients were diagnosed in the context of vascular insults proximal
ipsilateral MEPs may be secondary to incorrect set up of the to the pyramidal decussations or congenital disorders, using a
cranial or limb electrodes, and therefore technical issues should variety of methods (Table). Unlike other cases, our patient did
first be excluded.10 Subsequently, decussation anomalies can be not have any other structural brain anomalies.
assessed with trials of alternating bilateral and unilateral SSEP and DTI is a method for imaging the diffusion of water molecules
MEP recordings to demonstrate hemispheric origin.12 Ideally, this within the brain on MRI. Water molecules will preferentially
should be done before interpreting or monitoring evoked poten- diffuse along the length of an axonal structure (anisotropic
tials but this may be done at any time during the operation should diffusion), and this provides the basis for tractography using
the need arise.11,12 In our case, the correct lateralization of the diffusion MRI.22 In our case, DTI was used to visualize the corti-
monitoring leads and electrodes were verified intraoperatively, cospinal tract and to determine lack of decussation in the medulla.
and uncrossed corticospinal tracts were later confirmed to be the Similar methods have previously been used to visualize ipsilateral
cause using tractography. To the best of our knowledge, this is motor innervation.4,17,21
the first case of isolated ipsilateral motor innervation discovered Approximately 60% of axons in the corticospinal tract
incidentally with intraoperative monitoring during a neurosur- originate in the primary motor cortex.23 Fibers of the corti-
gical procedure. cospinal tract pass through the posterior limb of the internal

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IPSILATERAL MOTOR INNERVATION

in pyramidal decussation.16 The existence of individuals with


uncrossed pyramidal tracts raises fascinating questions into the
origins and evolutionary significance of pathway crossing in the
central nervous system.
The most comprehensive theory on why pathways cross the
midline was first articulated by Santiago Ramon y Cajal over 100
years ago.7,29 Cajal postulated that visual pathway crossing was
necessary to restore image continuity in the brain that would
otherwise be disrupted by image inversion through the lens.7,29
Sensory pathways then crossed to allow for a global representation
contralateral to the stimulus. Motor decussation then followed so
that ipsilateral sensory stimuli would activate motor function in
the ipsilateral limb. Indeed, the corticospinal tract is phylogenet-
ically a young tract found only in a few mammals capable of fine
motor movements.30 Computational models of 3-D spatial repre-
sentation have demonstrated a mathematical advantage for infor-
mation crossing in the central nervous system.31 Crossing allows
for faster processing speed, reduces the amount of information
necessary to impart somatotopy, and carries a lower likelihood
of miswiring errors from occurring compared with uncrossed
arrangements.31 Although a number of advantages to pyramidal
FIGURE 3. Postoperative axial fat-saturated T1-weighted MR image post-
decussation have been proposed, the existence of asymptomatic
gadolinium administration. Resection of the cerebellopontine angle and normally functioning individuals with uncrossed pyramidal tracts
internal auditory canal mass with a small amount of enhancing scar tissue suggests that pathways crossing in the central nervous system
is visualized (black arrow). may not be a necessary requirement for normal neurological
functioning.

capsule, the cerebral peduncle, and basis pontis and then 75%
decussate at the medullary pyramids to form the lateral corti- CONCLUSION
cospinal tract.24 Ten percent of axons remain uncrossed in the
ipsilateral lateral corticospinal tract and the remaining 15% form Nondecussated pyramidal tract is a rare congenital occur-
an ipsilateral uncrossed anterior corticospinal tract.25 Although rence that can either occur as part of a clinical syndrome or
human cadaveric studies have demonstrated substantial variations in isolation and without deficits. In isolated cases of uncrossed
in crossing patterns,26 lesions proximal to the pyramidal decussa- motor innervation, this congenital variant is only discovered
tions nearly universally cause contralateral extremity deficits. based on ipsilateral motor findings secondary to a unilateral struc-
The embryology of the corticospinal tracts has been eluci- tural injury proximal to the pyramidal decussations. Patients
dated with animal models and limited human studies.6 Layer V with uncrossed corticospinal pathways have been further inves-
neurons of the cortical plate extend projections distally during tigated with MRI, fMRI, transcranial stimulation for MEPs
embryogenesis and they continue developing postnatally, with and SSEPs, and visualized with DTI tractography. In this case,
myelination occurring within the first years of life.6,7 Decus- our patient was found to have ipsilateral motor innervation
sation at the medullary pyramids is completed by 17 weeks of incidentally discovered by intraoperative monitoring of MEPs,
gestation.6 A number of diffusible molecules mediate axonal and confirmed via DTI tractography. Given the increasing use
guidance toward midline and decussation. The absence of of intraoperative monitoring, this case underscores the impor-
netrin-1 or its receptor in mice causes impaired pyramidal decus- tance of cautious interpretation of seemingly discordant neuro-
sation.27 The Roundabout (ROBO) family of receptors are physiological findings. Once technical issues have been ruled out,
known to guide axons toward and away from the midline in ipsilateral motor innervation as a possible explanation may be
vertebrates.28 Interestingly, a gene mutation in ROBO3 was considered, and neurosurgeons should be aware of the existence
recently implicated in horizontal gaze palsy with progressive of this rare anatomic variant.
scoliosis, seminally linking the molecular underpinnings of axonal
guidance with human disorders of pyramidal decussation.16
In addition, in Situ hybridization has demonstrated abundant Disclosure
expression of this gene in the basis pontis of the human fetal The authors have no personal, financial, or institutional interest in any of the
brain at 15 and 19 weeks of gestation, consistent with its role drugs, materials, or devices described in this article.

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KU ET AL

FIGURE 4. A, DTI tractography in a coronal reformat, encoded such that blue fibers represent craniocaudal tracts,
red transverse, and green anteroposterior. This demonstrates lack of crossing of the corticospinal tracts (black arrows)
in the medulla. B, DTI composite image selectively showing the corticospinal tract in blue. Note that the tract remains
ipsilateral (white arrow). C, DTI tractography in a normal control subject for comparison, with crossing of portions
of the corticospinal tracts (black arrows).

TABLE. Cases of Ipsilateral Corticospinal Tract Reported In the Literature

Article Clinical context Other anatomical abnormalities

Cuatico (1979)13 Ipsilateral hemiparesis following left anterior cerebral artery occlusion None reported
for treatment of anterior communicating artery aneurysm. Ipsilateral
CST suspected based on clinical picture
Lagger (1979)14 Following death due to unrelated causes, ipsilateral CST visualized on Dandy-Walker malformation
postmortem serial sections of the brain stem and spinal cord in 2
patients with Dandy-Walker syndrome
Kudo and Uno (1984)15 Ipsilateral hemiparesis following ruptured middle cerebral artery None reported
aneurysm diagnosed with head CT and cerebral angiogram

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IPSILATERAL MOTOR INNERVATION

TABLE. Continued

Article Clinical context Other anatomical abnormalities

Hosokawa et al (1996)3 Ipsilateral hemiparesis following right internal capsule and Flat medulla on MRI.
thalamic hemorrhage. Ipsilateral CST confirmed with MRI Ipsilateral SSEP
visualization of Wallerian degeneration and with MEP
Terakawa et al (2000)5 Ipsilateral hemiparesis following right putamenal hemorrhage. Wedge-shaped medulla on MRI.
Ipsilateral CST confirmed with MEP and fMRI Ipsilateral SSEP
Jen et al (2004)16 Case series of patents with HGPSS. Ipsilateral MEP in all of the HGPSS.
patients assessed (n = 4) Pontine hypoplasia and “butterfly” medulla in
all patients assessed with MRI (n = 8).
Ipsilateral SSEP in all patients assessed (n = 4)
MacDonald et al (2004)12 Ipsilateral MEP in patient with HGPPS undergoing scoliosis HGPSS. Ipsilateral SSEP. Pontine hypoplasia
surgery and “butterfly” medulla on MRI
Mori et al (2005)17 In a patient with HGPSS, DTI visualized uncrossed right pyramidal HGPSS. Pontine hypoplasia
tracts and incompletely crossed left pyramidal tracts and “butterfly” medulla on MRI
Amoiridis et al (2006)18 Case series of patients with HGPSS. Ipsilateral MEP in all patients HGPSS. Ipsilateral SSEP
assessed (n = 2)
MacDonald et al (2007)19 Review of 206 spine surgeries with intraoperative monitoring. HGPSS. Ipsilateral SSEP
Ipsilateral MEP in 4 patients with HGPPS
Abu-Amero et al (2009)20 Case series of patients with HGPSS. Ipsilateral hemiparesis in HGPPS. Pontine hypoplasia and “butterfly”
1 patient following traumatic subdural hematoma. Ipsilateral medulla in all patients assessed with MRI
MEP in 7 patients with HGPPS undergoing scoliosis surgery (n = 5) Ipsilateral SSEP
Ng et al. (2011)4 Ipsilateral hemiparesis following left subcortical ischemic stroke. HGPPS. Pontine hypoplasia and “butterfly”
Ipsilateral CST confirmed with DTI medulla on MRI
Alurkar et al (2012)21 Ipsilateral hemiparesis following right subcortical ischemic None reported
stroke. Ipsilateral CST confirmed with DTI

CST, corticospinal tract; DTI, diffusion tensor imaging; HGPSS, horizontal gaze palsy with progressive scoliosis; MEP, motor evoked potentials; SSEP, somatosensory evoked poten-
tials.

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