380

J Neurol Neurosurg Psychiatry 1999;66:380–385

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SHORT REPORT

Parkinson’s syndrome after closed head injury: a

single case report
M Doder, M Jahanshahi, N Turjanski, I F Moseley, A J
Lees

Abstract
be evidence of midbrain damage or compres-
A 36 year old man, who sustained a skull
sion established at necropsy or by
fracture in 1984, was unconscious for 24
neuroimaging.4
hours, and developed signs of Parkinson’s
The only convincing examples of post-
syndrome 6 weeks after the injury. When
traumatic parkinsonism after acute closed head
assessed in 1995, neuroimaging disclosed
trauma that we have found in the literature are
a cerebral infarction due to trauma in-
the cases reported by Lindenberg5 and the
volving the left caudate and lenticular
report by Nayernouri.6 The first case of
nucleus. Parkinson’s syndrome was pre-
parkinsonism after an acute spontaneous in-
dominantly right sided, slowly progres-
tracranial haematoma, after rupture of a right
sive, and unresponsive to levodopa
middle cerebral artery aneurism, has recently
therapy. Reaction time tests showed slow-
been described.7 Well documented cases of
ness of movement initiation and execution
parkinsonism after a contralateral ischaemic
with both hands, particularly the right.
lesion of the striatum are rare. Fenelon and
Recording of movement related cortical
Houeto reported a case of non-progressive
potentials suggested bilateral deficits in
unilateral parkinsonism occurring a few
movement preparation. Neuropsychologi-
months after an ischaemic stroke.8 Brain MRI
cal assessment disclosed no evidence of
was suggestive of an ischaemic lesion in the
major deficits on tests assessing executive
territory of the left lenticulostriate arteries
function or working memory, with the
involving the entire striatum, apart from the
exception of selective impairments on the
fundus striati, and probably most of the lateral
Stroop and on a test of self ordered
pallidum.
random number sequences. There was
We now report a further case of Parkinson’s
evidence of abulia. The results are dis-
syndrome, which we consider to have occurred
The National Hospital cussed in relation to previous literature on
probably as a direct consequence of closed
for Neurology and basal ganglia lesions and the eVects of
head trauma.
Neurosurgery, Queen damage to diVerent points of the fronto-
Square, London, UK striatal circuits.
M Doder
Case report
(J Neurol Neurosurg Psychiatry 1999;66:380–385)
I F Moseley A
24 year old barman was involved in a road
A J Lees Keywords: parkinsonism; closed head injury; case
traYc accident in 1984. He sustained a skull
report
fracture and a fractured right arm, and was
Department of Clinical
unconscious for 24 hours with post-traumatic
Neurology, Institute of
Neurology, Medical
amnesia lasting several weeks. According to the
Research Council, Parkinson’s syndrome as a component of post-
patient and accessible medical notes he was in
Human Movements traumatic encephalopathy in boxers and Na-
hospital for 1 month, during which time he
and Balance Unit, tional Hunt steeple chase jockeys is well
received no neuroleptic drugs. Six weeks after
Queen square, recognised.1 A relatively pure “striatal” variant
the head injury, the patient noticed a coarse
London, UK of the punch drunk syndrome has also been
resting tremor, marked loss of dexterity, and
M Jahanshahi
occasionally described.2 However, very few
slowness in his right hand, and complained of
MRC Cyclotron Unit, convincing cases have been described after a
forgetfulness. Over the next 3 years there was
Hamersmith Hospital, single closed head injury. More than 50 years
little change in his symptoms, but in 1989 he
Ducane Road, London, ago, Crouzon and Justin-Besancon3 proposed a
started to drag his right foot and noticed a mild
UK set of minimum operational criteria for the
additional shaking of his right leg. Seven years
N Turjanski diagnosis of Parkinson’s syndrome secondary
after the accident, a mild resting tremor of his
Correspondence to: to acute head injury. They considered that the
left hand appeared and his speech was increas-
Dr AJ Lees, The National trauma should be severe and have led to
ingly slurred. Over the next few years a slow
Hospital for Neurology and concussion or unconsciousness, that there
progression of his parkinsonism occurred, with
Neurosurgery, Queen
Square, London WC1N
should be a close temporal relation between the
no response to levodopa or anticholinergic
3BG, UK. acute trauma and the onset of parkinsonian
therapy.
features, and that the course of the subsequent
In June 1995, he was seen at the National
Received 12 March 1998 and Parkinson’s syndrome should be uninter-
Hospital for Neurology and Neurosurgery.
in revised form
29 June 1998 rupted. Factor et al increased the stringency of
There was no history of previous exposure to
Accepted 9 July 1998 these criteria by insisting that there should also
dopamine antagonists. He smoked 10 cigarettes
Parkinson’s syndrome after closed head injury
381

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Figure 1 (A and B) MRI showing a well defined area
of abnormal signal adjacent to the frontal horn and anterior part
of the body of a slightly enlarged left lateral
ventricle, most probably a post-traumatic infarct.

a day and had drunk 30 units of alcohol a week

right hand with an associated postural tremor,
for the past 10 years. He was developmentally
and a mild resting tremor of his right leg and
dyslexic, and had attended a special school up
left hand. He had severe right sided lead pipe
to the age of 15, after which he had worked as a
rigidity with cogwheeling at the right wrist and
steeplejack and later as a storeman and then as
mild left sided stiVness. There was moderate
a barman. He had been right handed before the
bilateral bradykinesia and hypokinesia, worse
accident, but had subsequently switched to
on the right than the left, with striking
using his left hand for many dexterous activiti-
micrographia. He had absent right arm swing
es.There was no family history of Parkinson’s
and a slightly diminished left arm swing.
syndrome or essential tremor.
The fractured right arm was well healed by
On examination, he had an oblique scar in
the time of our assessment and there was no
the medial region of his forehead about 9 cm
residual loss of function.
long. He was alert and oriented, but was slow
There were no cerebellar signs, the plantar
to respond to questions. He had facial
responses were downgoing, and there was no
hypomimia, a markedly reduced blink rate with
evidence of autonomic failure.
a positive glabellar tap sign and occasional
Normal investigations included a full blood
blepharoclonus. Eye movements were full in
count, urea and electrolytes, fasting blood glu-
range, but he had diminished convergence and
cose, lipids, serum B12, thyroid function,
fine horizontal gaze evoked nystagmus to the
routine liver function tests, serum copper, and
left. His tongue was tremulous and his speech
caeruloplasmin. Wet blood film screening for
quiet and monotonous. There was a coarse pill
acanthocytes was negative and treponemal
rolling, 5 cycles/second, resting tremor of the
serological tests were also negative. His eryth-
382
Doder, Jahansahi, Turjanski, et al

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Figure 2 Positron emision tomography using 18F-dopa showing bilateral
reduction of putamen uptake.

rocyte sedimentation rate was 12 ml/hour and inferiorly to

the anterior part of the globus pal-
chest radiography, ECG, and EEG were lidus. There was
in addition a small focus of
normal. Slit lamp examination showed no similarly non-
specific abnormal signal in the
Kayser-Fleischer rings. white matter of
the anterior right temporal lobe,
Finally, an acute subcutaneous apomorphine associated with
minor shrinkage, presumed to
challenge and oral levodopa challenge tests represent
postcontusional encephalomalacia.
were negative, confirming dopaminergic unre- The remainder of
the cerebral hemispheres
sponsiveness. However, he developed chorei- seemed normal,
as did the midbrain and
form peak dose diskinesia in his right arm on infratentorial
structures (fig 1A and B).
increasing the dose of sinemet to 1000 mg daily A brain
perfusion SPECT study showed a
in January 1998. single
abnormality seen as an area of focal
reduction in
perfusion to the white matter close
Results to the left
basal ganglia. The perfusion ratios to
NEUROIMAGING
the grey matter
of the cortex and to the basal
Brain CT showed an area of low density, inter- ganglia on the
right hemisphere were within
preted as focal brain damage, in the left normal limits.
caudate nucleus, extending into the lentiform Positron
emission tomography using 18F-
nucleus, with ex vacuo enlargement of the dopa showed a
reduced uptake in the right
adjacent frontal horn. putamen (0.0055
Ki min-1) and normal cau-
On brain MRI this area was seen as a well date (0.0091 Ki
min-1) compared with control
defined area of non-specifically altered signal, values (caudate
0.0106+0.0019, putamen
slightly higher than that of CSF on all 0.0098 + 0.0011
Ki min-1). The 18F-dopa
sequences; it was concluded that this was most uptake on the
left side was also markedly
 probably a post-traumatic infarct. The lesion reduced,
however, the anatomical distortion,
involved the head and the anterior part of the induced by the
lesion made this result uninter-
body of the caudate nucleus, extending laterally pretable (fig
2).
into the anterior limb of the internal capsule,
reaching as far as the genu, and across to the
NEUROPSYCHOLOGICAL ASSESSMENT
anterior third of the putamen. It extended Our patient had
undergone neuropsychologi-
superolaterally into the centrum semiovale and cal assessment
on two previous occasions: the
Parkinson’s syndrome after closed head injury
383

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first in 1994, 10 years after the head injury, and
a few cases with suYcient evidence to implicate
the second 9 months after the first. The current
closed head trauma as an aetiological factor. It
assessment was performed 3 months after this
is possible that the rarity of reported cases
second assessment and included neuropsycho-
reflects the fact that head injuries severe
logical tests, of which we summarise only the
enough to badly damage the basal ganglia often
most relevant results.
lead to death.29 30 Mechanisms which may be
The Wechsler adult intelligence
relevant to the development of Parkinson’s
scale-revised9 indicated functioning at a low
syndrome after acute head injury include tear-
average to borderline level, reflecting a pattern
ing of small brain stem vessels by shearing
of ability which was longstanding and develop-
forces, direct traumatic injury to blood vessels
mental in origin. Reading and spelling tests10
leading to secondary thrombosis and infarc-
reflected dyslexic diYculties.
tion, and downward displacement of the brain
During the current assessment of memory
stem leading to contusion or haemorrhage.
functions, on the Rey auditory verbal learning
Tears occurring between the substantia nigra
test11 his immediate span was low for his age,
and surrounding structures and the cerebral
but probably in accord with his intellectual
peduncle may also be important pathogenetic
level. He showed some evidence of verbal
factors. It is also possible that morphological
learning, but also some loss of material after a
changes may not indicate the full extent of
delay of 45 minutes, with three false positives.
traumatic damage, but changes in neurotrans-
Performance was also assessed on some tests
mitter sensitivity and distal functional eVects
of executive function, such as the Wisconsin
may also be important.
card sorting test, Weigl sorting task, verbal flu-
We think that acute head trauma is the like-
ency, Reitan trail making, and Stroop test.12–16
liest aetiological cause for the Parkinson’s syn-
With the exception of the Stroop colour word
drome in our patient. There was a close
test16 there was little evidence of deficits on
temporal relation between the onset of symp-
tests of executive function or behavioural regu-
toms and the head injury which was severe
lation. On the Stroop test, interference was evi-
enough to leave radiologically demonstrable
dent during colour naming of 32 colour words
focal brain injury in the left lenticular nucleus.
written in incongruent ink compared with
The Parkinson’s syndrome progressed much
naming the colour of 32 coloured rectangles.
more slowly than expected for either Parkin-
We also evaluated our patient’s performance
son’s disease or another neurodegenerative
on tests of working memory which require
cause such as multiple system atrophy and
holding information “on line” and monitoring
there was no response to dopaminergic
responses. He showed a selective impairment
therapy. Functional imaging indicated that
on the test of self ordered random number
there was bilateral impairment of dopamine
sequences17 and similar to that for patients with
function in the nigrostriatal terminals, raising
Parkinson’s disease.18
the possibility that the head injury had caused
On the Beck depression inventory (BDI) he
more substantial damage than was evident on
obtained a score of 26.19
anatomical imaging. Bilateral reduction in

tracer uptake also raises the possibility that our

ASSESSMENT OF MOVEMENT PREPARATION,
patient’s symptoms might be consistent with
INITIATION, AND EXECUTION
idiopathic Parkinson’s disease, or that unilat-
Visual simple (SRT) and four choice (CRT)
eral structural damage (left caudate and
reaction time tasks were completed, as well as
lenticular nucleus in our patient) can cause
the Purdue pegboard and index finger
bilateral striatal dopaminergic dysfunction
tapping.18 20 On all these tests our patient
with retrograde degeneration of nigrostriatal
performed worse than an age matched healthy
terminals. Unilateral dopamine denervation
normal subject and similar to previously
models support the potential importance of
published data18 20 for elderly patients with Par-
dopaminergic interdependence between the
kinson’s disease. For both the SRT and CRT
two nigrostriatal systems.31–35 For example,
tasks his initiation times were slightly slower
bilateral striatal dopamine depletion induced
and his movement times considerably slower
by unilateral lesion dorsal to substantia nigra
with the right hand compared with the left.
was described in monkeys.35 The nigral
Movement related cortical potentials
dopamine was severely reduced on both sides
 (MRCPs) in our patient were compared with a
in the chronic experiments weeks after a
normal age matched subject, and the ampli-
unilateral caudate lesion in cats.34
tude of all components was reduced.21 The
From a meta-analysis of the 240 cases with
MRCPs before left hand movements had a
focal basal ganglia lesions reported in the
smaller amplitude and more delayed onset,
literature, Bhatia and Marsden36 concluded
with the early Bereitschaft Potential compo-
that Parkinson’s syndrome was exeptionally
nent possibly being absent, suggesting bilateral
rare, found only in 16 of the 240 cases (6%).
deficits in MRCPs.
Small (n=1) or large (n=4) lesions of the puta-

men, small (n=4) or large (n=1) lesion of the

Discussion
globus pallidus, or the lentiform nucleus
The association between acute head injury and
(n=3), and in one case a large caudate lesion. In
the development of a Parkinson’s syndrome has
the patient studied by us, such a predominantly
been an issue of controversial debate since
left sided subcortical damage was associated
James Parkinson’s essay in 1817.22 Although
with a mainly right sided parkinsonism. There
authors reported Parkinson’s syndrome after
was also slowness of initiation of movement
craniocerebral trauma,23–29 there have been only
and particularly movement execution quanti-
384
Doder, Jahansahi, Turjanski, et al

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by copyright.
fied on the reaction time tasks, and alterations This finding is
borne out by the case studied
of MRCPs. Such deficits have previously been by us. This patient was
assessed on a range of
reported for elderly patients with Parkinson’s tests considered to tap
“frontal” executive
disease.18–21 function. With the
exception of the Stroop test,
There is evidence of an asymmetry of motor there was little
evidence of deficits on tests on
eVects after cortical lesions. Wyke37 reported which patients with
idiopathic Parkinson’s dis-
that whereas dominant hemispheric lesions ease have been found to
be significantly
produced bilateral motor deficits, damage to impaired.20 Successful
performance on the
the non-dominant hemisphere aVected only Stroop test requires
development of a “percep-
contralateral limb movement. In our patient, tual set” for
suppression of the dominant
the bilateral nature of the deficits shown by the response of reading the
words to name the col-
reaction time tasks and MRCPs raises the our of ink of the
colour words printed in colour
possibility that subcortical motor structures incongruent ink. Our
patient had problems in
show a hemispheric asymmetry—similar to developing or
maintaining such a set. This was
that found after cortical damage. coupled with a
selective impairment on a
Abulia—that is, apathy with loss of initiative, specific test of
working memory, self ordered
spontaneous thought, and emotional random number
sequences, with relatively
responses—was found to be the commonest normal performance on
other tests of working
behavioural disturbance among 240 cases with memory, such as self
ordered pointing, random
focal lesions of the basal ganglia.38 number generation, and
missing digits. This
In light of this, our patient’s slowness in selective impairment on
a specific test of work-
responding to questions during the interview ing memory is
reminiscent of the results
and the high score on BDI are of interest. He reported by Robbins et
al,39 who studied a
had endorsed items reflecting loss of interest, young man with a left
striatocapsular infarct,
with a specific deficit
when “carrying out a
lack of enjoyment, diYculty in decision mak-
form of working memory
task in which the
ing, greater sense of fatigue, but absence of
subject has to ‘self-
order’ a series of responses
sadness.These suggest abulia rather than de-
using a self-generated
strategy”. These same
pression. Abulia is primarily a motivational
processes are also
involved in the self ordered
deficit that can impair performance of willed
random number sequences
on which our
actions. The surface manifestations of abulia patient was impaired.
can be similar to bradykinesia and akinesia, In monkeys, lesions
of the dorsolateral
which are motoric deficits. Therefore, it is pos- prefrontal cortex have
been shown to impair
sible that the slowness of movement initiation performance on tasks
involving non-spatial
and execution found in our patient by the reac- working memory
requiring monitoring and self
tion time tests, partly reflects the motivational ordered performance.40
The test of self ordered
deficits associated with abulia rather than the random number sequences
used in the current
motor slowness associated with bradykinesia. study has previously
been shown to activate the
The current assessment suggested some loss dorsolateral prefrontal
cortex in a PET study
of learnt material after a delay of 45 minutes. with healthy
participants.41
However, as impaired delayed recall was com- The finding that our
patient with damage
bined with correct delayed recognition of the predominantly to the
left striatum showed a
15 words, albeit with three false positives, this selective impairment on
this test, suggests that
suggests mainly retrieval rather than retention as the eVects of damage
to the prefrontal cortex
deficits. The cause of the memory problems are in the monkey,42 damage
to the striatum can
diYcult to determine. Focal lesions of the basal also produce deficits
in self ordered working
ganglia can be associated with retrieval memory.
deficits,39 and presence of abulia can contribute This is consistent
with previous evidence
to impairment of eVortful retrieval. Addition- that in the monkey,
similar deficits are
ally, in our patient MRI showed an abnormal produced on tasks such
as the delayed response
signal in the anterior right temporal cortex, and or object reversal
after lesioning the prefrontal
on that basis impairment on tests of non-verbal cortex or the striatum—
that is, at two diVerent
memory would be expected. Memory for non- points in the
frontostriatal loops.42 43 However,
verbal material was not included in the current our patient and the
case studied by Robbins et
assessment and the results of the two prior al,39 showed a specific
impairment of working
assessments of cognitive function were incon- memory in the absence
of major deficits in
sistent with regard to the presence or absence other tests of
executive function previously
of such memory deficits. found to be impaired in
patients with damage
Focal lesions of the basal ganglia do not to the frontal
cortex.44 This suggests that
result in uniform eVects on cognitive function. despite similarities,
in humans, the eVects of
Dubois et al38 concluded that in terms of cogni- striatal and prefrontal
lesions are not quantita-
tive function, lesions of basal ganglia are asso- tively or qualitatively
identical.40 44
ciated with normal intellectual eYciency,
preserved linguistic and spatial abilities, limited
The financial
assistance of the Welcome Trust (MJ) is gratefully
“frontal” dysfunction, memory retrieval deficit, acknowledged. We thank
Dr Patricia Limousin for providing the
and procedural learning disorders. They noted recording of MRCPs in a
normal subject and Dr D Costa from
Department of Nuclear
Medicine at Middlesex Hospital for
that the dysexecutive syndrome seen in patients carrying out the SPECT.
with basal ganglia lesions was less severe than
in patients with degenerative diseases of the 1 Foster JB, Leiguarda
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