Download Role of Cerebral Cortex in Voluntary Movements

Role of Cerebral Cortex in Voluntary Movements
A Review
PAUL D. CHENEY
Findings from studies using electrical stimulation of cortex, recording from single
neurons in awake animals, and measuring regional cerebral blood flow in humans
have revealed some specific motor functions for several cerebral cortical areas.
These areas include primary motor cortex, supplementary motor area, premotor
area, parietal areas 5 and 7, and prefrontal area. Execution of movement is a
function of the primary motor cortex, which translates program instructions for
movement from other parts of the brain into signals. These signals encode
variables of movement, such as the muscles to contract and the force and timing
of their contraction. Long-latency reflex responses of muscles to stretch and
cutaneous stimulation are also mediated by the motor cortex; other motor areas
seem to perform higher order motor functions. The supplementary motor area
controls input-output coupling in motor cortex and the programming of complex
sequences of rapidly occurring discrete movements, such as playing the piano.
The premotor area participates in the assembly of new motor programs. The
parietal areas 5 and 7 are involved in directing attention to objects of interest in
visual space and issuing commands for arm movements and eye movements to
these objects. The prefrontal cortex performs cognitive functions, such as shortterm memory of correct motor responses in delayed response tests.
Key Words: Brain, Motor cortex, Movement, Volition.
Early cortical stimulation experiments in human beings and animals
firmly established the motor function of
the primary motor cortex. In more recent work, motor functions have been
demonstrated for additional cortical
areas. The purpose of this article is to
review current concepts relating to the
functional roles offivedifferent cerebral
cortical areas in motor programming
and execution—primary motor cortex,
supplementary motor area, premotor
cortex, parietal cortex, and prefrontal
cortex. Emphasis has been placed on
aspects of cortical motor function that
may be relevant to physical therapy in
patients with cortical damage.
FUNCTION OF CORTICAL
AREAS
Overview
According to a scheme proposed by
Allen and Tsukahara, ideas for movements are translated into specific proDr. Cheney is Associate Professor, Department
of Physiology, University of Kansas Medical Center, Kansas City, KS 66103 (USA).
This work was supported in part by NIH grant
NS16262 and NSF grant BNS-8216608.
This paper was presented as part of the Motor
Control instructional course at the Fifty-Ninth Annual Conference of the American Physical Therapy
Association, Kansas City, KS, June 14, 1983.
This article was submitted November 21, 1983;
was with the author for revision 26 weeks; and was
accepted November 5, 1984.
624
grams by premotor association areas of
cortex (frontal and parietal areas), basal
ganglia, and the lateral hemisphere of
the cerebellum (Fig. 1).1 These programs
are then executed through the motor
cortex, which acts on brain-stem neurons and spinal motoneurons to bring
about the intended (desired) voluntary
movement. Of course, not all movements are completed as intended and
midcourse adjustments are sometimes
needed, for instance, when an obstacle
or unexpected change in load is encountered. In addition to these external perturbations of movement, internal factors, such as muscle fatigue, can also
cause a movement to deviate from its
intended course. Several feedback loops
exist to monitor the progress of the actual voluntary movement.1 One is the
visual system—a highly effective source
of feedback for reflex or volitional modification of movements under visual
guidance.2 Another source of feedback
is somatic receptors including cutaneous
receptors, joint receptors, muscle spindles, and Golgi tendon organs.3,4 These
receptors supply the CNS with continuous and prompt information about
limb position, muscle tension, and external stimuli. This information reaches
the intermediate division of the cerebellum, which is believed to use the information to make automatic corrections
for deviations from the course of the
intended movement. To do this, the
cerebellum is thought to compare information from somatic receptors about
the progress of the actual movement
with information from the motor cortex
about the intended movement.1 If these
differ, the cerebellum issues a correction
signal that acts through the motor cortex
and brain-stem descending systems to
return the movement to its intended
trajectory. In addition, information
from somatic receptors reaches the motor cortex through a more direct lemniscal pathway. Evidence now exists that
this pathway participates in reflexes elicited by muscle stretch and cutaneous
stimulation. These reflexes will be considered in more detail in a later section.
Figure 1 identifies four general aspects
of motor function: 1) motivation, 2)
ideation, 3) programming, and 4) execution. The phenomena of motivation
and ideation are not unique to motor
behavior but are components of a wide
variety of behaviors and, therefore, will
not be discussed further here. The programming and execution aspects of motor function will be the primary focus of
this paper.
Motor programming refers to neural
routines (communications) that convert
abstract ideas or thoughts about a desired movement into the proper strength
and pattern of muscle activity to bring
PHYSICAL THERAPY
PRACTICE
about the movement.5 The program
must specify the detailed sequence of
activity in different muscles, the force
each muscle should produce, and the
duration of its activity.
Movement execution has two components: 1) intention or the contribution of central commands to movement
and 2) feedback control or the modification of movement by signals from
sensory receptors. Execution is performed by the most peripheral components of the nervous system (final common pathways), including muscle, sensory receptors, and motoneurons. Cells
of descending systems that provide central "drive" to motoneurons, such as
corticospinal neurons, occupy an intermediate position between programming
and execution. These neurons translate
program instructions into motor commands in which the force of movement
is encoded by the cell's firing rate.6,7
I must emphasize that different types
of movements require different control
strategies. Although a functionally
meaningful subdivision of different
types of voluntary movements is difficult, the following list is suggested as
representing factors that pose different
control problems and that, therefore,
may require different central programs.
These categories, however, are not nec-
essarily mutually exclusive. Movements
may be classified according to
1. Their speed—slow (ramp), ballistic.
2. The number of joints involved—
simple (1 joint), compound (coordination of two or more joints).
3. The type of feedback guidance—somesthetic, vestibular, auditory, visual, some combination of these, or
none.
4. Their complexity (eg, the number of
discrete steps in a movement sequence).
5. The mechanism by which the movement is stopped—self-terminated or
externally terminated (mechanical
stops).
6. Accuracy constraints—absolute, relative, or none.
7. The degree of learning—most automatic or stereotyped (locomotion,
writing), least automatic (exploratory
activity with the hands).
The role of various forms of feedback
in motor control deserves further discussion. Two general models of motor
control have been proposed—closed
loop and open loop.8 Closed loop control involves the use of sensory feedback
signals from somatic, visual, and vestibular receptors to guide the movement
continuously and maintain the intended
trajectory. Corrections initiated under
closed loop control may be generated by
input from somatic receptors, which act
rapidly in a reflex manner to modify
motor cortex output, or by the visual
system, which acts more slowly and may
involve voluntary effort. Although the
closed loop mode of motor system function is well documented,8 open loop
control, in which movement execution
relies entirely on central preprogramming, may also apply in many situations
either because sensory feedback is ignored by the CNS or because the movement sequence is too fast to permit effective feedback correction. Examples of
such rapid movement sequences would
be batting a ball or playing the piano.
Even slower movements may be executed largely in open loop mode once
they have been thorougly learned
through repetition. Preprogramming
through practice and repetition may be
an important process by which motor
learning occurs.
WHAT AREAS OF CEREBRAL
CORTEX PARTICIPATE IN
VOLUNTARY MOVEMENT?
Areas of cerebral cortex involved in
voluntary movement have been identified by 1) motor deficits associated with
lesions, 2) neural unit activity related to
Fig. 1. Flow chart of interactions between the major brain areas involved in voluntary movement. An idea for a specific movement is translated
into detailed neural programs by basal ganglia, premotor cortical areas, and the lateral division of the cerebellum. These detailed instructions for
movement are then decoded and executed by motor cortex. Sensory receptors provide feedback about the actual movement to various levels
of the CNS, but particularly the intermediate cerebellum, which can compare this information with information about the intended movement and
initiate a correction if necessary. Premotor areas include supplementary motor area, premotor cortex, and parietal areas 5 and 7. (Adapted from
Allen and Tsukahara.1)
Volumes 65 / Number 5, May 1985
625
movement, 3) motor responses evoked
by electrical stimulation, and 4) meas­
urement of regional cerebral blood flow
in human beings. Cerebral blood flow
to a region is a measure of its metabolic
activity, which, in turn, varies with func­
tional (electrical) activity.9,10
Figure 2 is a sketch of the lateral
cortical surface of a monkey brain that
identifies different areas based on their
distinctive histological features (cytoarchitectonics).11,12 Areas that appear to
have a specific role in motor control are
given in Table 1.
TABLE 1
Cortical Areas Involved in Motor Control
and Their Corresponding
Cytoarchitectonic Designations
Fig. 2. Cytoarchitectonic map of monkey cerebral cortex. Different areas are distinguished
based on their distinctive histological appearance. Functional names corresponding to different
cytoarchitectonic areas are given in Table 1. Area 3, a subdivision of postcentral sensory
cortex, is buried in the bank of the postcentral gyrus. (Based on cytoarchitectonic scheme of
Vogt and Vogt,12 adapted from Wiesendanger.11)
Cytoarchitectonic
Field
Area
Motor cortex
Premotor
Supplementary motor
area
Prefrontal
Posterior parietal
4 (and 6Aα)
6Aβ (lateral part)
6Aβ (medial part)
9,10
5,7
Major Connections of Cortical
Motor Areas
Fig. 3. Major circuitry of the cortical motor system. Numbers indicate cytoarchitectonic areas;
Ml refers to primary motor cortex; SI to primary somatosensory cortex. Lines on the cortical
surface indicate major sulci. Ml is separated from SI by the central sulcus. (Adapted from
Wiesendanger.13)
626
The interconnections between brain
areas involved in movement can pro­
vide important clues about the func­
tional roles of these areas. Figure 3 sum­
marizes the major neural circuitry of the
cortical motor system.13 Within the cer­
ebral cortex, the general pattern of in­
formation flow from sensory input to
motor output seems to be from the sen­
sory systems to the parietal and tem­
poral association areas to the prefrontal
cortex to the supplementary motor area
(SMA) and premotor area and finally to
the motor cortex.11 In this organization,
the temporal and parietal cortex are sites
of converging input from the major sen­
sory systems. Although this is the pre­
dominant organization that emerges
from studying the interconnections of
major cortical areas, other more direct
routes to the motor cortex exist. For
example, parietal area 5 projects directly
to the motor cortex. In addition, frontal
or parietal association areas can influ­
ence the motor cortex through either of
two major reentrant loops—one involv­
ing the cerebellum and the other the
basal ganglia.
PHYSICAL THERAPY
PRACTICE
Figure 3 represents the motor cortex
as the only link between cortical areas
and motoneurons. Although the motor
cortex provides the brain with access to
motoneurons of virtually all somatic
muscles (excluding extraocular muscles), the phylogenetically older brainstem descending systems represent important and powerful additional inputs
to motoneurons through which the basal
ganglia, cerebellum, and cerebral cortex
may act, independent of the motor cortex, to influence movement. Furthermore, the premotor area and SMA have
direct corticospinal projections through
which they may influence motoneurons.
Nevertheless, in primates, which show a
high degree of encephalization, the motor cortex is clearly a key structure from
which descending command signals for
intended movements emanate.
Figure 3 also shows that the motor
cortex receives convergent input signals
from a multitude of sources. Central
input is received from several cortical
areas including premotor, SMA, parietal
area 5, and from two, major, central
reentrant loops.11 Motor cortex is also
influenced by two, major, sensory feedback loops. One of these (dorsal column
pathway) provides relatively direct feedback for use in reflex compensation; the
other (spinocerebellar pathway) goes
first through the cerebellum, which, in
turn, can alter activity in the motor
cortex or brain-stem descending systems. One of the roles of the motor
cortex is to transform these diverse input
signals, including sensory signals, into
appropriate output commands coding
which muscles should contract and at
what force.
MOTOR CORTEX FUNCTIONS
The motor cortex has been the most
extensively studied of all motor cortical
areas, and some of its properties are
relatively well understood. In general
terms, these functions involve the execution of intended movements and mediation of specific reflex responses. Specific functions may be summarized as
follows:
1. Decodes central program instructions from other cortical and noncortical areas and translates them
into specific output command signals that specify a) the muscles to
contract and relax (target muscles),
b) the force of contraction, and c) the
timing of contraction.
Volumes 65 / Number 5, May 1985
Fig. 4. Somatotopic representation of body parts (monkey) within motor cortex and supplementary motor area (SMA). This figurine map is based on movements evoked by electrical
stimulation of the cortical surface. (Adapted from Woolsey.16)
2. Informs other brain areas (cerebellum and basal ganglia) of the "intended" movement through corollary discharge.
3. Participates in long-latency components of muscle stretch reflex and
cutaneous grasp reflex.
Program Decoding and
Command Signals
How is the voluntary contraction of a
muscle specified by the motor cortex?
Work on both human beings and
monkeys14-16 has shown that motor cortex cells influencing different muscles
are arranged in an orderly fashion across
the precentral gyrus. For example, in
Figure 4, the image of a monkey's body
is superimposed on the surface of motor
cortex to show the relative location of
cells involved in movements of different
body parts. Two points relating to this
motor map should be emphasized. First,
the projection is largely contralateral,
that is, most motor cortex cells influence
muscle activity on the body side oppo-
site to the location of the cell. Second,
movements involving distal muscles are
represented by a much larger amount of
cortical tissue than those involving proximal muscles despite the fact that distal
muscles have a smaller mass. This disparity suggests a preferential role of motor cortex in distal movements.
Such somatotopic maps indicate a
general spatial separation of cells controlling movements at different joints,
but can individual muscles be selected
through the output circuitry of motor
cortex? Recent evidence demonstrates
that although some individual cortical
cells activate motoneurons of only a
single muscle, the majority of cortical
cells have more widely branching axons
and activate not one but a group of
synergist muscles.17 Nevertheless, the
motor cortex clearly provides the brain
with access to virtually all the body musculature and, in many cases, appears to
have adequate specificity for selective
activation of single muscles. Of course,
other components of the motor program
must channel activity to the appropriate
motor cortex cells.
627
FORELIMB
FL. EXT.
HINDLIMB
EXT. FL.
Fig. 5. Predominant action of motor cortex on flexor and extensor muscles of forelimb and
hindlimb in the baboon. F = facilitation; I = inhibition. Effects on ankle extensors are mixed;
the slowly contracting soleus muscle is inhibited from cortex, but the fast contracting gastrocnemius is facilitated. This correlates with the postural role of the soleus muscle. Effects on
elbow extensors are also mixed, but facilitation predominates. (Adapted from Preston et al.18)
Fig. 6. A. Types of synaptic organization between single motor cortex cells and motoneurons
of agonist and antagonist forearm muscles. B. Definition of agonist and antagonist muscles.
Agonist muscles are those whose activity increases with that of the cortical cell during voluntary
movement. U = cortical cell (unit) discharge; E = extensor muscle EMG; F = flexor muscle
EMG; POS = joint position.
Fig. 7. Typical relationship between firing rate of a motor cortex cell and maintained force.
Cells specify the force of movement by their frequency of firing.
The patterns of functional influence
exerted by the motor cortex on different
muscle groups can be examined at two
levels: first, the total or net effect of
motor cortex output on different motoneuron pools and second, the actions of
single motor cortex cells on different
motoneuron pools. The net output effects of motor cortex on forelimb and
628
hindlimb muscle groups have been determined by Preston et al,18 who used a
monosynaptic reflex conditioning procedure to test the effect of electrical stimulation of motor cortex on motoneuron
pools. Motor cortex stimulation can
either increase or decrease the magnitude of the summed discharge volley of
a motoneuron pool evoked by mono-
synaptic spindle Ia input. Increases represent net excitatory actions of motor
cortex on the recorded motoneurons;
decreases represent net inhibitory actions. Thefindingsfrom experiments in
primates are summarized in Figure 5.
The dominant pattern of motor cortex
action is different for different muscle
groups. For the hindlimb, muscles
whose contraction opposes the action of
gravity during static posture (all extensors of the hindlimb) are predominantly
inhibited by the motor cortex while the
flexors are predominantly facilitated.
This pattern is meaningful for understanding voluntary movement because
the initiation of a voluntary movement,
which is thought to be mediated by motor cortex, generally requires inhibition
of tonic antigravity postural mechanisms. For example, to initiate walking
from a standing posture, one leg must
flex at the hip, knee, and ankle while
the extensors of the opposite leg stiffen
to support the shift in load. The effects
on the forelimb in the monkey are more
complex and may reflect a transition
from quadrupedal to bipedal locomotion.
These findings can also be extrapolated to human beings and may help
explain some of the abnormal postures
observed in cases of cerebral damage.
Such patients typically exhibit extensor
rigidity in the leg and tonic flexion of
the elbow. If the motor cortex has a
tonic action in the absence of movement, with net effects resembling those
in Figure 5, then removing the motor
cortex input to motoneurons would release leg extensors and elbow flexors
from inhibition and would produce the
typical pattern of decorticate posturing.
A second, more refined, level from
which the motor cortex actions on muscle activity can be viewed is that of the
single cortical cell. Recently developed
techniques have enabled determination
of the types of effects single cells have
on agonist and antagonist muscles acting at a joint.19 Three major types of
cortical cells have been identified based
on the organization of their synaptic
inputs to forearm motoneurons (Fig. 6).
Cortical cells of one type facilitate muscles that they coactivate during voluntary movement (agonist muscles) but
have no effect on the antagonists; others
only suppress the antagonists and have
no effect on agonists. Still other cortical
cells have a reciprocal pattern of organization in which they simultaneously
PHYSICAL THERAPY
PRACTICE
facilitate agonists and inhibit antagonists.
How is the force and timing of muscle
contraction encoded? Force appears to
be encoded in the frequency of discharge
of corticomotoneuronal cells.6,7 The relationship in Figure 7 shows that the
maintained discharge of motor cortex
cells specifies the force of target muscle
contraction during steady holding
against a load. In addition, the firing of
many cells appears to encode the dynamic features of movement such as the
rate of force change.
The duration of muscle activity is determined by the duration of the motor
cortex cell activity that the motor program specifies. The activity of motor
cortex cells, however, begins slightly in
advance (60 msec) of muscle activity, as
would be expected for neurons that initiate muscle activity.
In conclusion, the muscles to be contracted in a movement are specified by
the set of motor cortex cells selected for
activation by the central motor program
and the distribution of synaptic connections between these cells and motoneurons. Furthermore, the motor cortex
cells encode in their activity the detailed
characteristics of movement, including
static force, rate of change of force, and
the timing of muscle activity.
Corollary Discharge to
Cerebellum
Corollary discharge to the cerebellum
is an aspect of motor cortex function
about which few details are known. The
basic theory, however, is that the cerebellum must have information about
the "intended" movement to compare
with the "actual" movement and to issue appropriate "error correction" commands. Therefore, a command for
movement from the motor cortex destined for motoneurons is transmitted
simultaneously to the cerebellum (Fig.
3). This "corollary discharge," as it is
called, is used by the intermediate division of the cerebellum to compare the
intended movement with the actual
movement and to make appropriate
corrections if an error is detected.1,20
Long-Latency Muscle Responses
to Stretch
The reflex responses of muscle to
stretch have been a subject of great interest in studies of motor control. The
existence of a spinal reflex mechanism
Volumes 65 / Number 5, May 1985
stretch reflex (M2) is almost as large
under passive conditions as when subjects are instructed to oppose actively
the perturbation.25 This suggests that
feedback from muscle afferents to sensorimotor cortex is improperly regulated
in Parkinson's disease so that the efficacy of transmission is always maximum.
Fig. 8. Spinal and transcortical stretch reflex loops. Minimal circuits for these reflexes
are shown at the left. Relative timing of muscle and cortical cell activity is indicated at the
right. Arrows plot the time required for afferent transmission from muscle to spinal and
cortical levels and efferent transmission from
cortical cells to muscle. The longer conduction distance for the transcortical loop results
in the longer latency of the M2 EMG peak
compared with the M1 peak. (From Fetz.23)
originating with muscle spindle afferents, which, in turn, excite motoneurons
directly, is well-established.3 The spinal
stretch reflex is a negative feedback
mechanism in which muscle stretch elicits a reflex contraction that opposes further lengthening of the muscle. Recent
data demonstrate the existence of a
transcortical stretch reflex pathway by
which the motor cortex contributes to a
longer latency of stretch reflex responses
of muscle (M2 in Fig. 8).21-23 Both the
spinal and transcortical pathways are
illustrated in Figure 8, which also shows
the relative timing of muscle responses
evoked by activity in each pathway. The
longer latency of the cortically mediated
reflex compared with the spinal reflex is
due to the additional conduction distance between spinal cord and motor
cortex.
Transmission through the transcortical reflex pathway is not obligatory but
rather depends on the subject's intended
movement. For example, the long-latency reflex is enhanced in a subject
instructed to resist an impending perturbation and is diminished or absent if
the instruction is to assist or ignore the
perturbation.24 The underlying instruction-related changes in the excitability
of CNS pathways made in preparation
for a voluntary movement are referred
to as "motor set."
The long-latency stretch reflex pathway may also be of clinical significance
because it is potentiated in Parkinson's
disease and may contribute to the rigidity associated with this disorder.21 Lee et
al reported that in Parkinson's disease,
the long-latency component of the
Cortical Mediation of the Grasp
Reflex
Lesions of SMA result in exaggerated
reflex grasping that can be elicited by
lightly stroking the glabrous skin of the
hand. This reflex is cortically mediated
because it is abolished by lesions of
either the sensory or motor cortex.
Moreover, the specific mechanism underlying the grasp reflex can now be
understood in terms of the input-output
coupling of motor cortex cells. Recordings from single motor cortex cells have
revealed a basic principle of input-output coupling.26 Cells whose electrical
stimulation produces movement in a
particular direction are also activated by
stimulation of the skin facing that direction. For example, motor cortex cells
mediating finger flexion are generally
activated by cutaneous stimulation of
the glabrous surface of the palm and
fingers. This circuitry, thus, forms a positive feedback loop for reinforcement of
grasping because contact between an object and the glabrous surface of the hand
will activate those specific motor cortex
cells that facilitatefingerflexors.This,
in turn, will strengthen the grip force,
further enhance cutaneous input from
the glabrous skin, and further increase
the activity of flexor motor cortex cells
(Fig. 9).
SUPPLEMENTARY MOTOR
AREA FUNCTIONS
Current evidence11,27 suggests that the
SMA is involved in two functions: 1)
control of input-output coupling in motor cortex and 2) assembly of motor
programs, specifically, the elaboration
of motor subroutines for rapid sequences of movements, such as those
involved in playing the piano, writing,
and speaking.
Control of Input-Output Coupling
in Motor Cortex
Evidence that the SMA is involved in
controlling input-output coupling in
629
TRANSCORTICAL GRASP REFLEX CIRCUIT
ments with a computer and displayed in
color-coded form on a video monitor.
The functional areas for which RCBF
measurements were made are labeled on
the Reference Brain in Figure 10. F. The
subjects were instructed to perform five
different motor tests. These tests are
fully described below, and the major
findings are summarized in Figure 10.
Motor sequence test. Subjects were
instructed to perform with eyes closed a
sequence of opposing movements with
the thumb and fingers. Within a 10second time period, the subject had to
touch briefly with the thumb the following fingers in succession: the index finger twice, the middle finger once, the
ring finger three times, and the little
finger twice. The sequence was then repeated in the reverse order. This task,
therefore, consisted of a rapid series of
discrete, low force, finger flexion-extension movements. Subjects were thoroughly trained before measurements
were made.
Fig. 9. Transcortical mechanism of the grasp reflex. Cutaneous receptors in the glabrous skin
of the hand activate motor cortex cells, which, in turn, flex the fingers.
motor cortex derives from observations
in human beings and monkeys that lesions of the SMA consistently produce
a hypersensitive grasp reflex so that light
tactile stimulation of the glabrous skin
on the palm of the hand or fingers produces an exaggerated, powerful reflex
grasp.11 The transcortical circuit for this
reflex was described in the previous section. Subjects are often unable to release
their grip on objects placed in the palm
of the hand. This control of the SMA
over input-output coupling in motor
cortex may also extend to proprioceptive transcortical reflexes (Fig. 8) because recent evidence has demonstrated
that stimulation of the SMA in monkeys
produces prolonged suppression of motor cortex cell responses to muscle
stretch.11 This finding also suggests a
possible explanation for the spasticity
that accompanies lesions of the SMA.28
If the SMA normally exerts some degree
of inhibitory tone over transcortical reflexes, destruction of the SMA would
allow these reflexes to operate at full
strength. Motor cortex cells show predominantly phasic responses to muscle
630
stretch, and enhancement of these responses after lesioning of the SMA could
contribute to the increase in resistance
to muscle stretch associated with spasticity.29
Programming of Movement
Sequences
Recent experiments in which regional
cerebral blood flow (RCBF) was measured in human beings during performance of different motor tasks have been
particularly revealing as to the functional roles of the SMA and other frontal
and parietal areas in voluntary movement.27,30 Regional cerebral blood flow
is proportional to oxygen consumption
and provides an indirect measure of total neuronal activity in an area.9,10 Roland et al injected 133Xe into the carotid
arteries of awake human subjects and
monitored its washout from different
areas of the cerebrum with 254 gamma
detectors surrounding one side of the
head.27,30 The RCBF for 254 separate
regions of each cerebral hemisphere
were calculated from these measure-
Repetitivefingerflexiontest. Subjects
compressed a spring held between the
thumb and index finger once every second. This test required more forceful
contractions than the motor sequence
test but was routine in that no complex
movement sequence was involved.
Internal programming of movement
sequence test. Subjects were asked to
simulate mentally the motor sequence
test but were instructed not to make any
actual movements (Fig. 10.A). Electromyograms confirmed that no muscle
activity occurred.
Maze test. Subjects were asked to
move the index finger in a specific pattern through a grid divided into 49
separate, 26- x 36-mm squares. Partitions separated adjacent squares. For example, in response to the verbal instruction, "move two forward, three left," the
subject was expected to move the index
finger two squares forward then three
squares left at a rate of one step every
second without skipping any squares.
This test, like the motor sequence test,
required memory of a movement sequence but differed from the motor sequence test and all other tests in that the
movement sequence changed with each
new verbal instruction and required
reassembly of the motor program. This
test also differed from the motor sePHYSICAL THERAPY
PRACTICE
quence test in that execution involved
use not only of finger muscles but also
of proximal arm muscles, and targets
were objects in immediate extrapersonal
space, that is, space surrounding but not
part of the body.
Spiral test. With ears plugged and
eyes closed, subjects drew in space with
the index finger (guided by compound
arm movements) a spiral of increasing
and then decreasing size. Subjects were
told to move about 120°/sec, make the
longest spiral about 75 cm in diameter
and the smallest about 2 cm; the number of turns was not crucial. This test,
like the motor sequence test and the
maze test, involved a complex sequence
of activity in the muscles. This test differed from the motor sequence test in
that 1) it required movement toward a
target object in extrapersonal space, 2)
it involved primarily use of proximal
limb muscles, and 3) its movements
were continuous with smooth transitions in activity from one set of muscles
to another. Because the subjects' eyes
were closed when the test was performed, target coordinates had to be
stored during training, recalled during
performance, and transformed into appropriate commands for muscle activity
just as in the maze test. This test differed
from the maze test in that 1) movements
were continuous rather than discrete
steps and 2) the required movement sequence remained unchanged during the
test.
Figure 10.A shows the cortical areas
that were activated during the motor
sequence test. Recall that the complex
sequence of movements in this test had
to be completed within 10 seconds and
left inadequate time to think about each
move. The movement sequence and
motor commands necessary to achieve
the movements had to be preprogrammed through experience during
which the subjects practiced the test. All
numbers in Figure 10 show the percentage increase in the blood flow to an
activated cortical area over the control
blood flow to the same area when the
subject was sitting quietly at rest. The
increases indicated by cross-hatching
were significant at the .0005 level, those
indicated by hatching at the .005 level,
and the outlined areas at the .05 level.
The medial surface of the hemisphere is
represented above each lateral view. Associated with the motor sequence test
(Fig. 10. A) were large increases in RCBF
to the hand area of primary motor corVolumes 65 / Number 5, May 1985
Fig. 10. Numbers represent increases in regional cerebral blood flow in human beings during
performance of various motor tests described in the text. A. Motor sequence test. B. Repetitive
finger flexion test. C. Internal programming of movement sequence test. D. Maze test. E. Spiral
test. F. Reference figure for identification of different cortical regions. Increases are averages
of several subjects and are expressed as percentages above control. Control measurements
were obtained with subjects sitting at rest with ears plugged and eyes closed; subjects were
instructed not to move or tense muscles and to "think of nothing." Experimental tests were
performed with eyes closed. Results shown are for the left hemisphere (tests A-D) and right
hemisphere (test E). Movements were all performed with the hand and arm contralateral to the
hemisphere shown. Both the lateral and medial (upper drawings) cortex are represented.
(Adaptedfrom Roland etal.27,30)
631
tex on the contralateral side (ipsilateral
motor cortex showed no change) and in
SMA, bilaterally. The increase in con­
tralateral primary motor cortex presum­
ably reflects increased neuronal activity
associated with the issuing of commands
for activity in specific finger muscles.
The finger representation of primary
sensory cortex on the contralateral side
also showed increased blood flow pos­
sibly as a result of increased sensory
input from the moving digits.
The bilateral increase in RCBF in the
SMA is most interesting. The increased
neuronal activity appears to be associ­
ated with some aspect of motor pro­
gramming because no increase in RCBF
was observed during repetitive, forceful
finger flexion-extension movements
that did not involve a specific planned
sequence (Fig. 10.B). In contrast, pri­
mary motor and sensory cortices did
exhibit increases during the simple flex­
ion test in Figure 10.B comparable to
those during the motor sequence test. A
role for the SMA in the planning of
movement sequences is further sup­
ported by the experiment in which the
motor task was internalized and the sub­
jects performed the movement sequence
mentally but were not allowed to exe­
cute any movements actually (Fig.
10.C). In the internal programming test,
the SMA but not the primary motor
cortex showed increased blood flow bi­
laterally, which suggests the SMA partic­
ipates in the assembly of programs for
ballistic movement sequences that occur
in rapid succession. Blood flow meas­
urements were not made during the
learning phase of this experiment. Dur­
ing this learning phase, however, infor­
mation about the types of movements
to be executed, the body parts to be
moved, and the sequence and timing of
movements must have been stored in
memory. Internal program execution of
the motor sequence test (Fig. 10.C) in­
volved recalling this information and
generating a set of time-ordered com­
mands. The formation of a motor sub­
routine specifying these aspects of
planned movement sequences, there­
fore, seems to be a major contribution
of the SMA. Even though the motor test
only involved muscles on one side, the
participation of the SMA in both hemi­
spheres confirms recent experiments in
monkeys showing that the activity of
single cells in the SMA is related to both
ipsilateral and contralateral move­
ments.31
632
TABLE 2
Classes of Neurons in Parietal Areas 5
and 7 of the Monkey
Neuron Type
Area 5
Joint rotation (passive)
Muscle (deep) receptors
(passive)
Cutaneous (passive)
Arm projection and hand
manipulation
Other
Area 7
Visual fixation
Visual tracking
Saccade
Arm projection and hand
manipulation
Visual only
Other and unidentified
%of
Sampled
Unitsa
64
14
9
11
2
27
7
17
15
18
16
a
Percentages compiled from work of
Lynch et al,36 Motter and Mountcastle,37 and
Mountcastle et al.35
Human speech is another type of
skilled movement that involves fast se­
quences of muscular contractions, and
RCBF to the SMA also increases during
speech.32 Presumably, movements such
as writing, typing, and playing musical
instruments also rely heavily on the
SMA.
Activation of the SMA was not lim­
ited to tests involving rapid sequences
of discrete finger movements, but also
occurred in the maze and spiral tests
that involved arm movements into extrapersonal space. These findings sug­
gest that the SMA also has a role in
controlling complex arm movement se­
quences. Further support for this hy­
pothesis derives from recent lesion ex­
periments in monkeys showing that uni­
lateral destruction of the SMA coupled
with corpus callosum lesions severely
impairs visually guided movements of
the contralateral hand.33
PREMOTOR CORTEX
FUNCTIONS
Premotor cortex refers to the lateral
part of area 6Aβ (Fig. 2). This appears
to be a secondary motor area unlike 6Aα
(the caudal part of area 6), which is part
of the primary motor cortex and con­
tains the representation of proximal and
axial muscles. Specific functions of this
area have been difficult to identify. Pre­
motor cortex can influence movement
by direct actions on motor cortex, by
actions on motor cortex through the
major reentrance loops, or by direct ac­
tions on brain-stem systems influencing
proximal and axial muscles (Fig. 3).1,11
Again, some of the most revealing
experiments on the function of the pre­
motor area have come from recent
measurements of RCBF in humans in­
structed to perform the specific motor
tests described earlier.27,30 The premotor
area did not show increased activity dur­
ing the motor sequence test (Fig. 10.A)
or during internal programming of
movement (Fig. 10.C); only a small in­
crease occurred during the spiral test
(Fig. 10.E). The dramatic increase dur­
ing the maze test, however, suggests that
the premotor area is involved in assem­
bling new motor programs as must have
occurred with each new instruction dur­
ing the maze test (Fig. 10.D). Because a
modest increase was also observed dur­
ing the spiral test, the premotor area
may also have some role in program­
ming arm movements into extrapersonal space.
PARIETAL CORTEX FUNCTIONS
Two parietal areas have been impli­
cated in motor control—area 5 and area
7 (Fig. 3). Area 5 is believed to be pref­
erentially involved in guidance of ex­
ploratory limb movements by tactile
stimuli, whereas area 7 is more involved
in visual feedback guidance of eye and
limb movements.34,35
Area 5 receives its principal input
from the primary somatic sensory cortex
and projects most heavily to the SMA
and premotor cortex (Fig. 3). Area 5
also sends some axons directly to the
spinal cord. Mountcastle et al,35 Lynch
et al,36 and Motter and Mountcastle37
have extensively investigated the prop­
erties of parietal neurons (Tab. 2). Most
neurons in area 5 are driven by simple
passive joint rotation (64%). A particu­
larly interesting class of cells comprising
11 percent of the sample (arm projection
and hand manipulation neurons, Tab.
2), however, discharged at high rates
only when the monkey reached for or
manipulated an object of interest (eg,
food for a hungry animal) in immediate
extrapersonal space. These neurons did
not respond to visual, auditory, or so­
matosensory stimuli and were unrelated
to similar movements in which no target
object of motivational interest was pres­
ent. Therefore, these neurons do not
directly encode simple movement charPHYSICAL THERAPY
PRACTICE
acteristics such as force, nor do they
respond to sensory stimuli; rather, they
seem to generate commands for the
manual exploration of targets of interest
in extrapersonal space.
What are the functions of area 7?
Electrical stimulation and unit recording experiments have shown that area 7
can be subdivided into three separate
regions—the first concerned with visual
guidance of arm movements, the second
with visual guidance of eye movements,
and the third with facial expressions.38,39
Area 7 differs from area 5 in its projections and afferent inputs. Area 7 receives
input from visual, somatic (through area
5), auditory, and limbic structures and
projects heavily to the prefrontal cortex
and to frontal eye fields— an area
known to be involved in control of eye
movements.40
The functional properties of cells in
area 7 are summarized in Table 2. As
expected, area 7 contains some neurons
related to arm movements and others
related to eye movements. An important property of a large fraction of area
7 neurons is that their discharge is contingent on the presence of objects of
motivational interest in immediate extrapersonal space.36 They seem to be
involved in directing attention to these
objects as targets for visually guided
arm-reaching movements or eye movements. Some neurons related to eye
movement are driven only by visual
input, others respond to both the visual
and motor aspects of the task, and still
others are related only to the motor
response.37,41,42 Neurons related only to
the motor aspect of the task may perform a command function bringing the
eyes to focus on objects of interest in
visual space (foveation). These "command" neurons can be subdivided into
three categories—visual fixation, visual
tracking, and saccadic (quick)—depending on the type of eye movement with
which they are related. Visual fixation
neurons discharge only during foveation
of stationary objects that are both of
interest and obtainable. For example, a
visual stimulus signaling the availability
of food activates these cells in a monkey
providing the food is within reach and
the monkey is hungry. The visual stimulus alone does not activate the cell
unless the stimulus has motivational significance to the monkey. Activation of
such cells, however, is visually dependent because blocking the view of the
object interrupts the cell's discharge.
Volumes 65 / Number 5, May 1985
Visual tracking neurons discharge during eye tracking (smooth pursuit) of
slowly moving, obtainable objects of interest in the visual field. The discharge
of individual neurons is maximal for
pursuit movements in a particular direction. Saccade neurons begin discharging
just before, and throughout, saccadic
eye movements toward objects of interest appearing abruptly in the peripheral
visual field. The activity of these cells,
however, is unrelated to spontaneous
saccades, such as those occurring in the
dark, or saccades toward visual stimuli
of no motivational interest. These properties suggest that parietal area 7 issues
commands for arm movements (like
area 5) and eye movements toward objects of motivational interest in immediate extrapersonal space. This is an important part of the more general process
of selective attention to specific environmental stimuli.
The deficits resulting from lesions of
parietal cortex in monkeys and human
beings generally reflect the properties of
parietal neurons as discussed earlier.
The major deficits with unilateral lesions can be summarized as follows:
1. Neglect of the contralateral arm including a reduction in spontaneous
and purposive movements and neglect of objects in the contralateral
visual field.43-45 These deficits are
most common in human beings with
lesions of the right (nondominant)
hemisphere.43
2. Difficulty in manipulating objects
with the contralateral hand
(apraxia).43
3. Astereognosis—failure to recognize
objects placed in the contralateral
hand.43,44,46
4. Errors in accuracy of arm movements.46,47 This is particularly severe
in the dark where proprioceptive
cues must be used to guide the limb
to its target. Errors in movements
made under visual guidance, however, are also easily detected.
5. Difficulty grasping an object with the
contralateral hand once it is contacted (primarily with lesions of area
5).47
6. Difficulty performing discrete hand
and finger movements requiring visual or proprioceptive cues.47 Bilateral
lesions produce deficits that are bilateral and more severe.
Cerebral blood flow measurements in
human beings also suggest a role for
parietal cortex in the guidance of arm-
reaching movements into extrapersonal
space.30 Only during the maze (Fig.
10.D) and spiral (Fig. 10.E) tests, which
were both performed with eyes closed
and presumably were guided by proprioceptive information, did the parietal
cortex "light up." Both these tests required a motor program that would
draw upon task-related information
generated during earlier experience to
assemble program instructions for accurate limb movement trajectories into
extrapersonal space. In these tests, the
eyes were closed so no object of motivational interest could be directly
viewed. In the maze test, however, hand
contact was made with the test board.
Because the test board possessed motivational interest for the subjects, its
manipulation may have activated hand
manipulation neurons in both areas 5
and 7.
PREFRONTAL CORTEX
FUNCTIONS
The prefrontal cortex influences
movement only indirectly (Fig. 3)
through projections to basal ganglia, cerebellum, and secondary cortical motor
areas. It receives afferents from limbic
structures (cingulate gyrus and amygdala), hypothalamus, thalamus, and
brain stem. These inputs presumably
convey to the prefrontal cortex information about the animal's motivations
and internal state.48 In addition, the prefrontal cortex receives visual, auditory,
and somesthetic information indirectly
through temporal and parietal association areas.11,48
Destruction of the entire prefrontal
cortex bilaterally produces a loss of motivation,48,49 a generalized dulling of
emotional behavior, and aimless hyperactivity. More restricted lesions limited
to the dorsolateral prefrontal cortex,
however, produce clear cognitive deficits in behavioral tests.50,51 These deficits consist primarily of disorders in attention to and short-term memory for
task-related cues. A clear correlate of the
short-term memory function of the prefrontal cortex has been identified in the
discharge of single prefrontal neurons
during performance of a delayed response task.48 In one such task, food is
placed under one of two identical objects in view of the monkey (cue phase).
View of the object is then blocked for a
period of about 18 seconds after which
the monkey must select the object containing food. A variety of firing patterns
633
Fig. 11. Unit discharge patterns in prefrontal cortex during delayed-response task.
Heavy lines (A, B, C, D, I, O) illustrate different
types of firing patterns observed in prefrontal
neurons during task performance. Upward
deflections indicate increases in firing rate.
Arrows indicate movements of an opaque
screen located between the monkey and test
objects. During the cue phase, food is placed
under one of the objects. The screen is lowered for about 18 seconds, then raised, and
the monkey must choose the object containing food. (From Fuster.48)
have been observed in single units during this task (Fig. 11). The discharge of
some units increased either transiently
(Fig. 1l.A) or throughout cue presentation (Fig. 1l.B). These cells may be involved in attention to the cue object.
Other cells (Figs. ll.C, D) showed a
sustained increase in activity during the
delay period (up to one minute) and
may constitute a short-term memory
apparatus. Over half of the cells in the
634
prefrontal cortex showed increased activity during the delay period; a small
number (8%) showed decreased activity
(Fig. 11.I). Neurons of untrained animals did not show delay-related activity.
Delay activation could easily be attenuated by distractions and was highly
related to the proficiency of performance. Additional tests, however, have
revealed that although activity during
the delay period is related to short-term
memory in some neurons, in other neurons, the activity is related to motor set
for an impending response.
In summary, findings from both lesion and unit recording experiments
strongly suggest a role for the prefrontal
cortex in short-term memory of cue features or location in delayed response
tasks. Additional roles of the prefrontal
cortex may include the processes of selective attention and motor set in preparation for an impending movement.
SUMMARY
Several cerebral cortical areas have
been shown to have a role in motor
control by the methods of electrical
stimulation, single unit recording in animals trained to make specific motor
responses, creating lesions of specific
cortical areas, and measuring RCBF in
humans. The areas are the primary motor cortex, SMA, premotor cortex, parietal areas 5 and 7, and prefrontal cortex. Neurons of the primary motor cortex encode the detailed characteristics of
movement such as the desired force of
muscle contraction and its timing.
These signals are then transmitted directly to motoneurons. Motor cortex,
therefore, executes program instructions
for movement by transforming input
signals into signals that encode movement characteristics. The primary motor cortex also participates in reflex responses of muscle to stretch and cutaneous stimulation (grasp reflex). The
SMA is involved in the programming of
complex sequences of discrete movements occurring in rapid succession,
such as piano playing. The SMA also
appears to exert control over the efficacy
of input-output coupling in transcortical
reflexes evoked by muscle stretch and
tactile stimulation. Parietal area 5 is
strongly influenced by somatic and kinesthetic input from the limbs and appears to issue motor commands for tactile exploration of extrapersonal space
with the hand. Parietal area 7 is more
strongly influenced by visual input than
somatic input. Its function seems to be
one of selective attention to objects of
motivational interest in extrapersonal
space by issuing eye movement commands for foveation of such objects and
for arm movements to them. The prefrontal cortex may perform multiple
functions, but one of these appears to
be the cognitive function of short-term
memory in delayed response situations.
A large variety of different types of
movements can be identified based on
factors such as speed or degree of training. Different types of movements place
different demands on the neural control
system. Hence, the degree of involvement of different cortical areas in movement will vary widely depending on the
specific requirements of the movement
performed.
Acknowledgment. I thank Linda Carr
for typing this paper.
PHYSICAL THERAPY
PRACTICE
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