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REVIEW ARTICLE
Summary
Bradykinesia means slowness of movement and is one
of the cardinal manifestations of Parkinsons disease.
Weakness, tremor and rigidity may contribute to but do
not fully explain bradykinesia. We argue that
bradykinesia results from a failure of basal ganglia output
to reinforce the cortical mechanisms that prepare and
execute the commands to move. The cortical deficit is
most apparent in midline motor areas. This leads to
particular difficulty with self-paced movements,
prolonged reaction times and abnormal pre-movement
EEG activity. Movements are often performed with
normally timed EMG bursts but the amount of EMG
activity is underscaled relative to the desired movement
parameters. There are also abnormalities in sensory
scaling and sensorimotor integration. The brain appears
Introduction
The term bradykinesia was first used by James Parkinson to
describe one of the cardinal features of the disease that
now bears his name. It is now recognized, however, that
bradykinesia may be part of the motor dysfunction in many
movement disorders.
Bradykinesia is often used synonymously with two other
terms: akinesia and hypokinesia. Strictly speaking,
bradykinesia describes the slowness of a performed
movement, whereas akinesia refers to a poverty of
Oxford University Press 2001
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Muscle weakness
Several studies (Stelmach and Worringham, 1988; Stelmach
et al., 1989; Jordan et al., 1992) have compared the strength
of patients with Parkinsons disease and healthy age-matched
subjects. All of them found a mild reduction of strength in
a variety of muscle groups, even though this sometimes
failed to reach statistical significance. One probable reason
for this lack of agreement is that it is difficult to match
patient and control groups for the amount of daily exercise
and diet.
A recent study by Corcos and colleagues attempted to
resolve this problem by measuring strength at the elbow in
patients when ON and OFF L-dopa following overnight
withdrawal of therapy (Corcos et al., 1996). When OFF
medication, there was a 30% reduction in the strength of
maximum elbow extension and a 10% decrease in elbow
flexion. Because intrinsic muscle properties could not have
changed in the short period between the OFF and ON
conditions, the difference in strength must have been due to
an inability of patients to activate the elbow muscles
maximally. In that study, the patients appeared to be highly
motivated to produce strong contractions when OFF and ON
therapy, so that lack of volitional drive was not thought to
be a factor. A later study by Brown and colleagues on the
wrist extensors showed that one physiological reason for the
reduction in strength is the persistence of action tremor
during maximal contraction (Brown et al., 1997). Tremor at
~10 Hz in patients OFF therapy prevents maximum fusion
of motor unit contraction and can contribute to weakness.
However, this cannot account for the decrease in strength in
all muscle groups, so that other, presumably central, factors
must also be involved. The conclusion is that patients with
Parkinsons disease can be weak in some muscle groups and
this will inevitably contribute to slowness of movement.
Rigidity
Long-latency stretch reflexes are enhanced in Parkinsons
disease (Tatton and Lee, 1975; Berardelli et al., 1983;
Rothwell et al., 1983). They could potentially contribute to
bradykinesia if they were elicited in an antagonist muscle
during an active isotonic contraction of the agonist. Johnson
and colleagues tested this hypothesis by using a torque motor
to stretch muscles unexpectedly during active sinusoidal
movements of the wrist (Johnson et al., 1991). They showed
that reflexes elicited in the antagonist muscle were not
suppressed as much as in normal subjects, and that the
degree of abnormality was related to the amount of clinical
bradykinesia. The one flaw in this argument was that the
amount of activity in the antagonist muscle during
unperturbed flexion/extension movements was no greater
than that seen in normal subjects. Thus, there was no evidence
in the actual movements tested that antagonist co-contraction
could have been a limiting factor. Indeed, co-contraction has
never been described as an important feature even in very
rapid movements, in which the triphasic ballistic movement
EMG pattern has been analysed in some detail. The conclusion
must be that the role of rigidity in bradykinesia has yet to
be proven conclusively.
Movement variability
The movements of patients with Parkinsons disease are less
accurate than normal, particularly if they have to move as
fast as possible (Sanes, 1985; Sheridan and Flowers, 1990;
Phillips et al., 1994). In other words, the speedaccuracy
trade-off is less efficient in patients than in healthy subjects.
Sheridan and Flowers suggested that bradykinesia might be
due to an active strategy of patients to move more slowly in
order to improve their accuracy (Sheridan and Flowers,
1990). Although this is a plausible strategy, other factors
must also be involved since bradykinesia remains in tasks
in which spatial accuracy constraints have been removed
(Teasdale et al., 1990).
Bradyphrenia
Slowness of thought, or bradyphrenia, could lead to
bradykinesia by interfering with movement planning and, for
example, increasing reaction time. Whether bradyphrenia
exists in Parkinsons disease has been controversial. In part,
this is due to the fact that many patients with Parkinsons
disease do develop dementia from several aetiologies, and
there is certainly slowing of thinking in dementia (Berry
et al., 1999). Additionally, there is slowing of thought in
ageing and depression (Cooper et al., 1994), and these factors
need to be considered. Lastly, many cognitive studies have
employed procedures that have required a motor response,
so that bradykinesia might cause an apparent bradyphrenia
(Rafal et al., 1984). Confusion has arisen from a number of
studies that have not taken these factors into consideration.
Moreover, thinking is not just one process and whether it is
slow might depend on the nature of the task. Some studies
have claimed to find bradyphrenia (Cooper et al., 1994; Pate
and Margolin, 1994), but most have not (Rafal et al., 1984;
Duncombe et al., 1994; Howard et al., 1994; Spicer et al.,
1994). It is likely that bradyphrenia is not responsible for
slowing when dementia is not present and the patient is not
on drugs, such as anticholinergics, that might interfere with
cognitive processes.
Primary bradykinesia
Although all the factors above can contribute to bradykinesia,
they must be distinguished from the core disorders of
central movement control that are responsible for primary
bradykinesia. In this section we describe those features of
bradykinesia that cannot be explained by secondary factors.
Bradykinesia could potentially be due to slowness in
formulating the instructions to move (programming) or to
slowness in executing these instructions. Although
programming and execution are usually thought of as separate
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Fig. 1 (A) Premotor potentials preceding self-initiated movements for normal subjects (continuous line) and patients with Parkinsons
disease (broken line). (B) Premotor potentials preceding externally triggered movements for normal subjects (continuous line) and
patients with Parkinsons disease (broken line). The mean time of stimulus presentation is 253 ms prior to EMG onset for patients with
Parkinsons disease and 212 ms for normal subjects. Pre-movement EEG activity was normal in patients with Parkinsons disease when
they performed an externally triggered task compared with the reduction that is seen in self-paced movements. From Jahanshahi et al.,
1995.
and Marsden, 1999). This effect was specific for the motor
areas involved in the motor task and correlated with the
improvement of bradykinesia. Wang and colleagues reported
similar findings in their study of simple and complex
movements (Wang et al., 1999). The above studies suggest
that the basal ganglia have a role in releasing cortical elements
from idling rhythms during voluntary movement. In a recent
report, Brown carried this idea one stage further by examining
the effect of dopaminergic stimulation on the coupling of
activity between different nuclei of the basal ganglia (Brown
et al., 2001). They recorded local potentials from patients
with implanted electrodes in the subthalamic nucleus and
internal pallidum, and found that they were coupled by
activity at 2030 Hz when the patients were OFF medication,
whereas ON medication this changed to 6070 Hz.
Motor execution
Single ballistic movements at a single joint
Single movements made as fast as possible about a single
joint are slower than normal in patients with Parkinsons
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triphasic EMG pattern in which the time and duration of the
bursts varies in a highly predictable way depending on the
amplitude and other parameters of movement. This pattern
is present in patients with Parkinsons disease, but the first
agonist burst is small. As Hallett and Khoshbin pointed out,
the result is that patients often add further bursts of EMG to
the pattern in order to achieve enough force to move the
limb to the required end position (Hallett and Khoshbin,
1980). Despite this, if patients aim for a movement of larger
amplitude, the size of the agonist burst can increase. In
effect, this means that the size of the agonist burst is not
always a limiting factor in slowing movement: if the burst
for the large movement had been used for the smaller
movement the speed would have been normal. The conclusion
is that there is a second cause of bradykinesia in simple
movement: inappropriate scaling of the dynamic muscle force
to the movement parameters (Berardelli et al., 1986b).
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Transcranial stimulation
Sensorimotor processing
Some authors have reported abnormalities in sensorimotor
processing in Parkinsons disease. Schneider and colleagues
reported a decrease of precision in two-point discrimination
and proprioceptive position sense (Schneider et al., 1986)
and Klockgether and colleagues, in a study of arm movements
testing the effects of both visual and kinaesthetic information,
suggested that peripheral afferent feedback is impaired in
patients with Parkinsons disease (Klockgether et al., 1995).
A problem in matching somatosensory and visual inputs was
demonstrated by Demirci and colleagues (Demirci et al.,
1997). The authors postulated that this was due to an
abnormality of sensory scaling and drew parallels with the
abnormal scaling of motor output reported by Berardelli and
colleagues (Berardelli et al., 1986b).
A deficit in sensorimotor integration may also be observed
in precision grip/lift tasks. These are complex acts that are
performed by gripping an object with the correct amount of
force so that it does not fall between the fingers when it is
lifted off a supporting surface. Parkinsonian patients take
longer to develop peak grip force and show a pronounced
slowing in the rate at which grip force is generated. They
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Fig. 3 Mean motor-evoked potential (MEP) area in normal subjects and in patients with Parkinsons
disease at various stimulus intensities and degrees of muscle activation. In Parkinsons disease, the slope
of the inputoutput relationship between stimulus intensity and response size was steeper than normal.
From Valls-Sole` et al., 1994.
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Conclusion
The term bradykinesia is often used to cover a range of
related problems in the control of movement. However, in
all cases the principal deficit is that movements are slow.
The data reviewed here suggest that, although secondary
factors such as muscle weakness, tremor and rigidity may
contribute, the principal deficit is due to insufficient
recruitment of muscle force during the initiation of movement.
The result is that patients movements undershoot their targets
and end by approaching it in several smaller steps. The two
distinguishing features of parkinsonian bradykinesia are (i)
that patients underscale muscle force and (ii) that the deficit
is often ameliorated when external cues (vision, sound) are
given to guide the movement. The former has led to the
suggestion that bradykinesia is a problem of scaling motor
output appropriately to the task rather than to any intrinsic
limitation in motor execution. The latter is usually interpreted
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Received August 10, 2000. Revised May 5, 2001.
Accepted May 31, 2001