Brain (1986), 109,293-305

HYPOMETRIA WITH HEMISPATIAL AND LIMB
MOTOR NEGLECT
by KIMFORD J. MEADOR, ROBERT T. WATSON, DAWN BOWERS and
KENNETH M. HEILMAN
{From the Department of Neurology, College of Medicine, University of Florida, and the Veterans
Administration Medical Center, Gainesville, Florida, USA)

SUMMARY
A patient with a haemorrhage in the right mesial frontal lobe exhibited hypokinesia, bradykinesia
and a hypometric movement disorder of his contralateral limbs. This movement disorder was
characterized by reduced amplitude of otherwise normally formed movements (hypometria). In
addition, the left limb hypokinesia improved with placement of the left forelimb into right hemispace
(hemispatial motor neglect). We postulate that the hypokinesia, bradykinesia and hypometria were
induced by reduction in activation of forebrain dopaminergic and basal ganglion motor systems,
which in conjunction with the supplementary motor area are critical for setting the activational level
for motor output.
INTRODUCTION

The mesial frontal lobe contains the supplementary motor area (SMA) and the
cingulate gyrus. Penfield and Welch (1949, 1951) introduced the term SMA to
designate a cortical region just anterior to the primary motor foot area. Electrical
stimulation of this region may induce inhibition of voluntary motor activity (e.g.,
speech arrest), vocalization (vowel cry or 'cri de l'aire motrice supplemental'),
contraversing of the head and eyes with tonic raising of the contralateral arm,
complex manoeuvres and postures of the limbs on both sides, or occasionally
autonomic responses and sensory experiences (Penfield and Welch, 1949, 1951;
Talairach and Bancaud, 1966; Wiesendanger, 1981). Deficits after unilateral SMA
or cingulate lesions, or both, are for the most part transient (Penfield and Welch,
1951; Watson et al., 1973; Laplane et al., 1977). In the acute phase, patients have
global akinesia that is much more prominent in the contralateral extremity along
with hypotonia and grasp reflex. Severe impairment of spontaneous speech has
been found to accompany isolated lesions of either the left or right mesial frontal
lobe (Masdeu et al., 1978; Brust et al., 1982). Lesions involving the SMA and
cingulate gyrus have been reported to induce a neglect syndrome (Heilman and
Valenstein, 1972; Damasio et al., 1980). In addition, isolated lesions of the anterior
Correspondence to: Dr Kimford J. Meador, Department of Neurology, Medical College of Georgia, Augusta,
GA 30912.
© Oxford University Press 1986

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cingulate gyrus in monkeys have also been reported to induce neglect (Watson et
al., 1973). Within a few weeks after a mesial frontal lesion, remarkable recovery
generally occurs and the only lasting significant motor deficit reported is
dysdiadochokinesia of the contralateral limbs (Penfield and Welch, 1949; Laplane
etal., 1977; Wiesendanger, 1981).
We describe a man who had a haemorrhage into the right SMA and anterior
cingulate gyrus. In addition to the aforementioned deficits, the patient had a
contralateral hypometric movement disorder (i.e., reduced amplitude but otherwise
normally formed movements of the left forelimb). Although slow initiation of
movement in the contralateral limb has been reported to follow SMA lesions, the
hypokinesia in our patient was noted to improve when his left hand was placed on
the right side of his body. In other words, the hypokinesia varied with body
hemispace (hemispatial motor neglect). In addition, the left limb hypokinesia was
more profound when cued by stimuli on the right side or when performing bilateral
simultaneous movements (motor extinction) (Valenstein and Heilman, 1981).

CASE R E P O R T
A 64-year-old right-handed man with hypertension and coronary atherosclerotic disease suddenly
experienced severe right-sided headache, difficulty in speaking, and inability to use his left arm and
leg. He was alert and orientated for person, time and place. Digit span was normal. His remote
memory was intact, but recent memory was mildly impaired for verbal and spatial items. Naming,
repetition, comprehension and speech prosody were normal. Word fluency was decreased, and he
had particular difficulty initiating speech. The patient read normally, but made occasional syntactic
errors when writing. He also made several spelling errors. Finger agnosia, acalculia and right-left
confusion were not present. Praxis was normal in the right hand, but initially could not be tested in
the left hand because of the akinesia. Remarkable improvement in the left limb akinesia was noted
when he was given a bimanual task with a real object such as opening a jar or putting on a glove.
After several days, the akinesia improved and he could perform unimanual tasks with the left hand,
although he remained slow in initiating movement. Mild dysdiadochokinesia and decreased fine
motor movements with the left hand were noted. For simple visually guided movements, such as
touching the examiner's finger or raising the arm to shoulder level, the patient could make full
movements. However, when tested on a series of more complex manual praxis items (e.g., imitating
the use of a key, scissors or a hammer), the most pronounced deficit was a 20 to 80 per cent
reduction in amplitude of the components of movement with the left forelimb. For instance, when
asked to pantomime hammering with each hand, he moved his left wrist slightly as opposed to full
excursions with his right forelimb. The spatial and temporal features of these slowly initiated small
amplitude movements were normal or only very minimally altered. Stereognosis, graphaesthesia,
and visuospatial construction were intact. Double simultaneous stimulation disclosed no sensory
extinction. That the patient had difficulty performing the following tests was suggestive of frontal
lobe dysfunction: Luria figures, letter sequencing, fist-edge-palm, and go/no-go tasks (Stuss and
Benson, 1983). In addition, he exhibited a general inertia and impersistence. Examination of the
cranial nerves revealed no abnormalities. Decreased tone was noted in the left arm and leg. As the
akinesia resolved, mild left hemiparesis (greater in the leg than in the arm) was noted. Although
hypokinesia and bradykinesia (i.e., slow movement after initiation) were most prominent on the left,
they were also present on the right. The tendon reflexes were hyperactive on the left. The plantar
response was flexor on the right and equivocal on the left. A left grasp reflex could be

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FIG. A, routine uncontrasted CT scan on day of onset of symptoms showing haemorrhage in the region of the
SMA. B, three weeks later, follow-up contrast-enhanced CT in a plane between coronal and transaxial planes
showing the depth of extension into the anterior cingulate gyrus.

elicited. Computed tomography (seefig.)showed a right mesial frontal haemorrhage in the region of
the SMA and anterior cingulate gyrus with a very slight shift of the midline structures.
RESULTS

Special Neuropsychological Testing
We performed neuropsychological tests to explore further the patient's deficits
and to elucidate their neuropsychological mechanisms.
The Western Aphasia Battery (Kertesz, 1979) confirmed that the patient had
decreased fluency with good comprehension, naming and repetition. This symptom
complex has been termed 'transcortical motor aphasia' (Benson, 1979).
To learn whether the patient recognized that his own movements were
hypometric, we repeated several praxis test items, and the patient was asked
whether he thought that the amplitude of each movement was appropriate in size.
Despite persistent left hand hypometria, he stated that the amplitude appeared
correct on all items. To learn whether a proprioceptive defect could account for
this hypometria, the examiner then performed the same movements using various
amplitudes; the patient selected the correct amplitude. Although this finding was
consistent with a proprioceptive defect, with his eyes closed the patient could
discern the correct amplitude when his left arm and hand were passively moved
through the same items at various amplitudes. He therefore had knowledge of the
correct amplitudes, and his disorder could not be attributed to a proprioceptive
defect. To learn whether the hypometria was limited to previously learned skilled
movements, the examiner moved the patient's left hand passively, tracing a line,
circle or large letter while the patient's eyes were closed. Reproduction of each
movement by the patient was hypometric. In addition, with his eyes open, simple
repetitive movements such as finger tapping were hypometric.

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approached, but did not reach, statistical significance in the control group: RTs in
left space (X = 296.1 ms) tended to be faster than those in right space (X = 298.1
ms), and this pattern is opposite that obtained by the patient (i.e., right space less
than left space).
A significant main effect for Task (¥\\t) = 145.8, P < 0.00001) was also found
for the patient; bimanual RTs (X = 1019.1 ms) were significantly slower than
unimanual RTs (X = 681.1 ms). For the control group, however, there were no
differences between bimanual (X = 297.5) and unimanual (X = 296.6) RTs (Fi 4
= 0.05, P < 0.83).
For the patient, there were also significant interactions between Hand x Task,
Hand x Space, and Space x Task (see Table for summary of F-values). Post hoc
comparisons of the Handy. Task interaction using Duncan's procedure showed
the following. (1) For both the unimanual and bimanual conditions, RTs of the
left hand were significantly slower than those of the right hand (unimanual-left
hand = 796.7 ms, right hand = 565.9 ms, P < 0.01; bimanual-left hand =
1347.9 ms, right hand = 690.3 ms, P < 0.01). However, the discrepancy between
the RTs of the two hands was markedly greater for the bimanual condition (105 %
increase in RT from the right hand to left hand) than for the unimanual
condition (46 % increase in RT). (2) For both the right hand and left hand,
bimanual RTs were significantly slower than unimanual RTs (right hand-bimanual
= 690.3 ms, unimanual = 565.4 ms, P < 0.01; left-hand-bimanual = 1347.9 ms,
unimanual = 796.7 ms, P < 0.01). However, the left hand appeared dramatically
slower by the bimanual condition (as reflected by a 69 % increase in RT from the
unimanual condition) than was the right hand (22 % increase in RT from
the unimanual to bimanual conditions). This same Hand x Task interaction
approached, but did reach, significance in the control group (Fj 4 = 6.3, P =
0.065). The pattern of performance suggested that the normal subjects, like the
patient, tended to have slower left hand than right hand RTs in both the unimanual
and bimanual conditions.
Significant Space x Task interactions were obtained for both the patient and the
control subjects (see Table for summary of F-values). Post hoc comparisons
(Duncan) disclosed the following. (1) The patient showed no difference between
RTs in left (X = 701.1 ms) and in right space (X = 661.0 ms, P > 0.05) in the
unimanual condition. In contrast, normal subjects had faster RTs in left (X =
293.5 ms) than in right space (X = 299.1, P < 0.05) in the unimanual condition.
(2) For the bimanual condition, the patient's RTs in right space (X = 951.3) were
faster than those in left space (X = 1086.9, P < 0.01), whereas the normal subjects
showed no difference between RTs in left and in right space in the bimanual
condition (left = 298.6 ms, right = 296.5 ms, P < 0.05). (3) For both the patient
and the controls, unimanual RTs were faster than bimanual RTs within left
space (patient-unimanual = 701.1 ms, bimanual = 1086.9 ms, P < 0.01; normal
subjects-unimanual = 293.5 ms, bimanual = 298.6, P < 0.05). (4) The patient
also showed faster unimanual (X = 661.0 ms) than bimanual RTs in right space

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(X = 951.3 ms, P < 0.01). However, the control subjects showed the opposite,
that is, faster bimanual than unimanual RTs in right space (bimanual = 296.5,
unimanual = 299.1, P < 0.05).
Finally, a significant Hand x Space interaction was found for the patient, but
not for the controls. Post hoc comparisons (Duncan's) showed: (1) left hand RTs
were significantly faster in right (X = 981.6) than in left hemispace (X = 1162.9,
P < 0.01), whereas right hand RTs were comparable across right and left space
(right = 630.6, left = 625.0, P < 0.05); (2) for both left and right space, right
hand RTs were faster than left hand RTs (left space—right hand = 625.0, left
hand = 1162.9, P < 0.01; right space—right hand = 630.6, left hand = 981.6,
P < 0.01).
The major findings thus include the following. (1) The patient had both right
and left limb hypokinesia, in that his right and left hands were significantly slower
across all tasks as compared with the performance of normal subjects. (2) In
general, the left hand was slower than the right for both patient and normal
subjects, but the magnitude of the percentage of difference between right and left
hands was considerably less for the controls and suggested that compared with
controls the patient had left-hand hypokinesia. (3) Although both the patient and
normal subjects had slower left hand than right hand RTs on the unimanual tasks,
only the patient had slower left than right hand RTs for the bimanual task. Both
the patient and normal subjects had slowing of the right hand for the bimanual
task compared with the unimanual task, but only the patient had slowing of the
left hand on the bimanual task. This finding is consistent with motor extinction
(Valenstein and Heilman, 1981). (4) The patient's left hand was faster in right
than in left hemispace for both unimanual and bimanual tasks. Normal subjects
had no such hand x space interaction; however, they were faster in left hemispace
for the unimanual task. These findings suggest that although the patient had a
predominantly left limb hypokinesia, this deficit varied with hemispace.
DISCUSSION
This patient showed several movement abnormalities. He had generalized
akinesia and bradykinesia that were primarily contralateral. Although these
symptoms have been previously reported to occur with lesions of the mesial frontal
lobe (Penfield and Welch, 1951; Talairach and Bancaud, 1966; Wiesendanger,
1981), ours is the first reported case of contralateral hypometria and of hemispatial
motor neglect from a mesial frontal lesion. The patient also exhibited motor
extinction and increased difficulty initiating isolated left limb movement when
stimulated on the right side.
Our patient's hypometric movements occurred only with movements guided by
internal representations. For these types of movements to be made, there must be
an engram that directs the strength, duration, speed and temporal sequence of
activation and relaxation in specific muscle groups. The decreased amplitude of
our patient's left arm movements could not be attributed either to a simple

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proprioceptive defect or to a loss of the knowledge (engram) of the proper
movement amplitude, because he recognized the correct amplitude when his limb
was moved passively. The question may then be raised why he did not correct his
movement by comparing it to those engrams. Bizzi et al. (1976) postulated that in
simple movement, the nervous system specifies the correct joint position (i.e.,
target position) through the selection of a set of length-tension curves in the
agonist and antagonist muscles. Since we have shown that our patient did have
knowledge of the target position, his hypometria could result from an improper
selection of the length-tension curves. This postulate, however, fails to explain not
only why his movements were hypometric rather than dysmetric (inappropriately
large or small in amplitude) but also why he was slow to initiate movements and
slow in the speed of his movements once initiated.
Hypokinesia, hypometria and bradykinesia all accompany dysfunction of the
basal ganglia and the mesocortical forebrain dopaminergic systems. The
importance of the forebrain dopaminergic systems in movement is highlighted by
experimental animal studies in which akinesia may be induced by bilateral
destruction of ascending dopaminergic pathways or by drugs that block dopamine
receptors (phenothiazines and butyrophenones), inhibit dopamine synthesis (alphamethylparatyrosine), or prevent dopamine storage (reserpine). In contrast, motor
activity may be increased in animals given drugs that release dopamine
(amphetamines) or act as dopamine agonists (apomorphine) (DeLong and
Georgopoulos, 1981). These findings suggest the involvement of dopaminergic
systems in our patient. Further evidence lies in the fact that almost all the previous
clinical reports of limb hypometria concern patients with Parkinson's disease. In
this disease, hypometria, bradykinesia, hypokinesia, or a combination of the three
is evident in proximal limb movements (Wilson, 1925), ballistic limb movements
(Angel et al., 1970; Flowers, 1976), tracking (Cassell et al., 1973; Flowers, 1978),
repetitive movements (Schwab et al., 1959), ocular saccades (Jones and DeJong,
1971), micrographia (McLennan et al., 1972), hypophonic speech and 'petit pas'
gait (Wilson, 1925).
Kinnier Wilson (1925) believed that these symptoms resulted from a 'deprivation
of, or a serious reduction in, normal impulses to movement'. He pointed out that
such a poverty of movement could arise from lesions at one or more neural levels
in the jacksonian sense, and that at the 'highest' level, transcortical impairment
could produce a dimunition of the 'will' to act. Evarts and Tanji (1974) provided
electrophysiological evidence in monkeys that the motor cortex can be gated by
the voluntary set. Set-related activity (intentional activity) has been observed in
SMA (Tanji et al., 1980); and, the 'BereitschaftspotentiaF (BP), a readiness
potential that precedes the cortical motor potential, has its largest amplitude at
the vertex over the SMAs (Deecke and Kornhuber, 1978). In hemiparkinsonism,
the amplitude of the BP is reduced over the affected hemisphere preceding any
movement and reduced bilaterally, preceding movements of the akinetic extremity
(Deecke et al., 1977). It therefore appears that the SMAs are necessary for normal

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function of intentional systems (i.e., those systems involved in the preparation and
activation of a motor response). The SM As have strong somatosensory input and
access to motor integration at multiple levels (Kiinzle, 1978; Brinkman and Porter,
1979; Damasio and Van Hoesen, 1980; Wiesendanger, 1981; Brust et al., 1982).
Schell and Strick (1984) have suggested that the main influence on motor output
occurs at the cortical level. Thus the SMA is at a strategic position in transmitting
striatal and dopaminergic influences onto motor output.
Any coordinated movement is the product of a specific pattern of motor neuron
firing. The regulation of neuronal synthesis leading to voluntary movements may
occur at any level of nervous integration from cortical to spinal neural assemblies
(Dow, 1969); however, the frontal lobes have been regarded as particularly
important in the regulation of complex forms of motor operations due to their
analysis and integration of the products produced by several sensorimotor regions
(Bianchi, 1895; Luria, 1980). The SMAs are a part of the frontal systems which, in
conjunction with the ascending dopaminergic tracts, are critical for activation
leading to purposeful movements. The cingulate gyrus appears to be a part of
these activational systems, in that isolated lesions of the cingulate gyrus in monkeys
induce a neglect syndrome (Watson et al., 1973). In man, the relative roles of the
SMA and cingulate gyrus remain uncertain because of the simultaneous
involvement of the SMA and cingulate gyrus according to most reports and
because of the lack of cases with isolated unilateral cingulate lesions. Isolated
bilateral stereotactic cingulumotomies are reported in the setting of psychosurgery
(Foltz, 1977), but the neuropsychological aspects of motor activation have not
been well studied in this group.
Just as the mesencephalic reticular formation has an important role in generalized
cortical arousal (Moruzzi and Magoun, 1949), the ascending dopaminergic tracts
appear to be involved in tonic activation of intentional systems. Selective intention
is mediated to a large degree by the activity of the SMAs in a frontocortical
system, which interacts not only with the basal ganglia and ascending dopaminergic
tracts but also with the thalamus (specifically VLo, VLm, centromedianparafascicularis, and nucleus reticularis thalami) (Scheibel and Scheibel, 1967;
Yingling and Skinner, 1977; Watson et al., 1981; Weinrich et al., 1984). Disruption
of neuronal synthesis in the network forming the intentional system leads to a
failure of motor activation (Deuel and Collins, 1984).
Although the akinesia and bradykinesia in our patient were bilateral, they were
much more prominent in the limb contralateral to the lesion. Slight mass effect on
the contralateral SMA may have influenced the bilateral dysfunction. However, in
normal subjects complex sequential unilateral limb movements produce increased
cerebral blood flow to both SMAs (Roland et al., 1980a, b), which sugests that
directed unilateral limb movement is initiated by the conjoined action of both
SMAs. That the motor deficits are more pronounced in the contralateral limb
suggests that although the SMAs work synergistically, the ipsilateral SMA is
dominant for systems in that cerebral hemisphere. While ipsilateral dominance is

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the normal functional state, the circuitry for bilateral integration exists (Kiinzle,
1978) and provides a substrate for the functional recovery that ultimately develops
after most unilateral SMA lesions (Penfield and Welch, 1949; Laplane et al., 1977;
Wiesendanger, 1981).
Motor extinction has been attributed to the effects of reciprocal inhibition and
to the effects of limited capacity (Valenstein and Heilman, 1981). Because our
patient was touched on the right, this signal may have prepared the left hemisphere
for action and reciprocally inhibited the already poorly activated right hemisphere.
The right hemisphere could not reciprocally inhibit the initial activation of the
right hand. Alternatively, the left SMA may be mediating intentional systems for
both hemispheres. The solitary SMA has limited capacity and cannot prepare
both sides for action simultaneously. With right body stimuli, there is an automatic
activation of the left hemispheric motor systems, which preferentially discharge
before that of the right.
In our patient, the major intentional deficit was a predominantly left limb
hypokinesia; however, we also showed a less marked but significant effect of
hemispace, in that placing the left limb into right body hemispace improved the
hypokinesia. Heilman (1979) and Heilman and Valenstein (1979) postulated that
each hemisphere mediates attention and intention towards and in contralateral
hemispace independent of the extremity used. Placing the hypokinetic left limb in
right hemispace may have improved the hypokinesia in our patient because this
manoeuvre further activated the left cerebral hemisphere, which was responsible
for preparing movement of the left arm in the absence of the right SMA. That is,
the increased left cerebral activity, and increased left SMA activity in particular,
improved the driving of residual right motor systems.
While sequential movements, including speech, are being executed or even
imagined, xenon cerebral blood studies show that activity of both SMAs increases
(Larsen et al., 1977; Lassen et al., 1977; Roland et al., 1980a, b). In contrast,
execution of simple repetitiveflexionsor sustained isometric muscular contractions
is not associated with increased SMA metabolism. These findings led Roland
and colleagues to hypothesize that the SMAs are not supplementary but are
'programming areas for subroutines and that these areas form a queue of timeordered motor commands before voluntary movements are executed by way of
the primary motor area'. However, the function of the right and left SMAs are
different. Although function of the left SMA is consistent with Roland's hypothesis,
the right SMA does not appear to be involved in the same manner with the primary
motor programs. For example, our patient with the right SMA lesion exhibited
marked hypometria and hypokinesia with otherwise normally formed movements.
We postulate that the right SMA is critical for setting the activational level for
motor output and that hypokinesia and hypometria were produced by reduced
activation. Although the left SMA is involved to some lesser degree in motor
activational (intentional) systems, it seems to be more involved in sequencing the
primary motor programs. In our experience (Watson et al., 1986), patients with

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left SMA lesions have milder akinesia, more severely decreased word fluency, and
no hypometria. However, they do exhibit classical apraxia in both hands. Thus
the right SMA may be more important for the initiation and amplitude of
movements, whereas the left is more important for the spatial and temporal
features of the movements.
ACKNOWLEDGEMENT
This study was supported in part by National Institutes of Health Grant NS20204 and by the
Medical Research Service of the Veterans Administration.

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