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J. S. Taube
Neural Representations of Intended
Movement in Motor Cortex
The motor cortex consists of a number of functionally
and connectionally interrelated areas that participate
in the planning and production of voluntary move-
ments. Functions like conditional association, co-
ordinate transformation, and linking of movements
occur in multiple parietal, cingulate, and frontal areas.
There is a general organization that abstract aspects of
planning and spatial organization occur in parietal
cortex, while sequencing and execution of movement
occurs in frontal areas. However, these functions are
extensively intermingled across the set of motor areas,
so that intended movements are products of continual
interactions across a broad region of cerebral neo-
cortex.
1. What is the Motor Cortex?
The cerebral neocortex is frequently considered to be
the primary site where voluntary movements are
planned, initiated and, to some extent, learned. These
ideas have been supported by studies using a variety of
methods, including single and multiple neuron record-
ing, lesion effects, and human functional brain imaging
(Sanes and Donoghue 1997). This body of work has
significantly advanced our understanding of the means
by which plans for voluntary movement are assembled
and used for muscle control. This article will define the
term motor cortex and the cortical areas that comprise
it, then describe how various motor areas participate
in voluntary movement. Our present knowledge leads
to the conclusion that a vast cortical territory co-
operates in fashioning voluntary movements from
external cues or mental intentions.
The motor cortex comprises a collection of more or
less distinct areas or fields, which are united by
function and connectivity. A field is typically, but not
exclusively, included as motor if neurons in that area
modulate their discharge in close conjunction with the
contraction of voluntary muscles, it receives inputs
from other motor structures in the central nervous
system (CNS) and it contributes output through the
corticospinal tract. More detailed differences in the
functional properties, connections, and cytoarchitec-
ture distinguish one motor area from its neighbors.
Ongoing anatomical and functional studies of frontal
and parietal cortex add to a progressively increasing
list of motor separate cortical fields; probably more
than a dozen can be identified. The blending of sensory
and motor properties across the neocortex means that
many cortical fields could be classified within several
different domains, pointing out the vagaries of forcing
divisions in a region of the CNS that is inherently
integrative. Among motor fields, oculomotor and
somatomotor control areas are often separated. This
review deals with those areas of cortex that control the
somatic musculature, in particular those involved in
arm reaching movements, which have been most
thoroughly studied.
1.1 Subdiisions of Motor Cortex
Figure 1 summarizes the regions where neurons related
to arm reaching are likely to be present in the human
brain. Localization of motor areas in humans is
inexact because their identification is based upon data
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Neural Representations of Intended Moement in Motor Cortex
Frontal Parietal
cs
MI ips
SPL
PMd
SI IPL
PMv
Te
Lateral view
cs
preSMA
SMA
CMA
cing s
Oc
Medial view
Figure 1
Human cortical motor areas. The general regions where
neurons related to intended movements are shaded in a
lateral (top) and medial (bottom) view of the human
brain. The frontal and parietal lobes are separated by
the central sulcus (cs): Primary motor cortex lies in the
precentral gyrus anterior to the cs, while the somatic
sensory cortex (SI) is situated in the postcentral gyrus
posteriorly. The superior and inferior parietal lobes
(SPL, IPL), separated by the intraparietal sulcus (ips),
probably contain multiple motor areas based on data
from non-human primates. Frontal motor areas include
the premotor ventral (PMv) and dorsal (PMd),
supplementary and presupplementary areas (SMA,
preSMA). The cingulate cortex region also contains
multiple motor areas (CMA), which are located along
the cingulate sulcus (cing s) (Oc, occipital lobe; Te,
temporal lobe)
obtained directly from single neuron recordings in
non-human primates. Similar data is difficult to obtain
in the normal human brain. Localization is made by
correlating areas of blood flow changes from imaging
techniques in humans with a presumed homolog in
other species. Traditionally, the primary motor cortex
(MI, Brodmanns area 4), which is located on the
precentral gyrus of many primates (including hu-
mans), is considered a primary site for movement
10560
generation. It is ranked primary largely because
movements of the opposite side of the body can be
elicited by the lowest levels of electrical stimulation
anywhere in the cortex. Among cortical areas, MI also
has the bulk of the direct projections to the spinal
cord, including some direct projections to alpha motor
neurons (" 5 percent). In addition, MI neurons are
active with voluntary movement, and lesions of MI
lead to paralysis of the contralateral musculature.
Lying in front of MI are a collection of frontal lobe
non-primary areas, where stimulation thresholds are
higher, neurons may have more complex properties,
and lesions result in movement defects other than
frank paralysis, such as incoordinations called
apraxia. While there is some diversity in the naming of
these other motor areas, a dorsal and ventral premotor
(PM), a supplementary motor (SMA), and pre-
supplementary motor area (pSMA) are commonly
recognized as distinct areas; each of these may be sub-
divided further (Geyer et al. 2000). More recently it
has become apparent that the cortex on the medial
wall of the cerebral hemisphere along the cingulate
sulcus is related to movement planning and pre-
paration (CMA; Strick et al. 1998), which also appears
to contain multiple subdivisions.
The parietal lobe can be subdivided into a number
of areas associated with somatic sensation in its
anterior part (SI or primary somatic sensory cortex),
and for all senses more posteriorly. The posterior
parietal cortex is divided into superior and inferior
lobes which, on the basis of non-human studies, is
likely to contain multiple somatic motor areas. The
parietal lobe is heavily engaged in spatially guided
actions. In the anterior parietal cortex, the postcentral
gyrus contains a collection of four distinct somatic
sensory areasBrodmans areas 3b,1, 2, and 3a. The
former two areas seem mainly concerned with proces-
sing of touch, while areas 2 and 3a process deep or
kinesthetic information from the joints, muscle spin-
dles (muscle length and velocity), and golgi tendon
organs (muscle tension receptors). Neurons related to
the production of arm movement are also in this
region, particularly in area 2. More posterior areas of
parietal cortex (both IPL and SPL) contain areas
related to eye and arm movement, often blended with
various types of visuo-spatial or other sensory mo-
dality related neurons. In monkeys, group areas
related to reaching and grasping movement are located
in the intraparietal sulcus; whether such areas are in
the same location in humans is not resolved. Most
posteriorly in the parieto-occipital area, the PO region
of monkeys is an additional arm related area; also
termed V6 for its visual responsiveness (Burnod et al.
1999).
1.2 Connections of Motor Areas
Motor areas are densely interconnected with each
other and with other cortical areas; the thalamus and
 Neural Representations of Intended Moement in Motor Cortex
the basal ganglia, brainstem and, for most areas, the
spinal cord. All motor cortical areas are interconnec-
ted within at most two or three synaptic relays, but this
is also true of most of the CNS, making connectivity
difficult to be used as a sole differentiator of dedicated
motor areas. Direct connections exist from parietal to
frontal lobes with a general pattern that regions close
to the central sulcus (dividing SI and MI, see Fig. 1) in
the parietal cortex project to regions close to the
central sulcus in the frontal cortex, creating a rough
pattern of mirror symmetry of connections (see review
of Geyer et al. 2000). It is essential to emphasize the
vastly parallel nature of possible interactions among
motor areas, rather than any simplistic view of a
stepwise serial process from one to the next area.
Beyond the clear picture of vast interconnectivity of
areas, studies of the timing of neurons during move-
ment planning and action demonstrate that neurons in
most or all of the motor areas interact extensively
(Wise et al. 1997).
2. Cortical Areas Engaged in Moement Imaging
Methods
A broad perspective of the activation patterns of
motor areas can be gained from brain imaging studies.
Both positron emission (PET) and functional mag-
netic resonance imaging (fMRI) studies in humans
show that primary motor cortex is engaged when
voluntary actions are produced. By contrast, pre-
motor and supplementary motor areas can be
activated simply by planning motor actions, although
they are also engaged during movement production
(Sanes 2000). Recently, human cingulate cortex has
been tied to movement based on activation in PET and
fMRI studies. Cingulate motor areas (CMA, Fig. 1)
can be activated by grasp and reaching actions; some
functions may be segregated within rostral and caudal
cingulate areas (Picard and Strick 1996). Other results
suggest that cingulate cortex may play a role in
performance monitoring and in selection of actions
(Carter et al. 2000). Similarly, the parietal lobe is
heavily engaged in voluntary arm movements when
viewed by brain imaging methods. Numerous areas
of the parietal lobe activate with arm movement
(Connolly et al. 2000), suggestive of multiple sub-
divisions, as reported in monkeys (see later).
3. Actiity of Single Neurons in Cortical Motor
Areas
Single neuron recordings in nonhuman primates give
the most direct evidence for the role of cortical areas in
movement. In addition, they verify conclusions based
upon the indirect PET and fMRI measures. Neuronal
activity has been measured during movement planning
by instructing movement first, then, after a delay,
requesting its enactment (an instructed delay task)
during movement sequences and after various aspects
of kinematics and dynamics have been varied. Neuron
activity has been correlated with direction, amplitude,
various types of loads, sequence structure, and
sensory-motor contingencies and attention. Rather
than describe the patterns of neural activity in each
area under each of these conditions, only general
patterns of engagement of each area will be described.
One of the most pronounced features of motor cortex
neurons is the relationship of firing modulation to
direction of a reaching movement.
Neurons in frontal and parietal areas are direc-
tionally tuned so that they fire most to one direction
and less so to other directions, and typically are least
modulated in the direction opposite to their preferred
direction. Neurons in motor areas are also modulated
by force, and kinematic features (amplitude, position,
and velocity changes) (Kalaska et al. 1997, Fu et al.
1993, Ashe and Georgopoulos 1994). Each of these
features is correlated with neuronal activity, but causal
links to the actual computation of these aspects of
movements are less certain. The current experimental
data cannot fully dissociate whether or where con-
version from an abstract notion of movement in space
to muscle activity patterns occurs. However, the
relatively weaker influence of movement force on
neural activity in the parietal areas suggests that motor
plans are more abstract here, compared to the frontal
lobe.
Correlation of force and neural activity is common
in MI, but many neurons are influenced by kinematics
as well, so that there is no clear cut neuronal
segregation of these features. The activity of neurons
during motor preparatory delays has provided further
evidence for a role in planning actions. Neurons with
delay activity are found across motor cortex, but they
are more prevalent in the nonprimary regions. How-
ever, other work also suggests that even primary
motor cortex may be involved in cognitive aspects of a
motor plan (Carpenter et al. 1999), so it is difficult to
accept a simple notion that plans are formulated in
nonprimary cortex and then passed to MI for com-
mand generation. Rather, the set of areas continually
cooperate throughout the planning and production of
movement. This does not negate the finding that
certain functions predominate in specific subdivisions
of the motor cortex.
4. ParietalFrontal Engagement in Moement
It is clear from electrophysiological, lesion, and imag-
ing data that the computations concerning the spatial
coordinates of movement are processed in the parietal
lobe, while movement execution is more weighted
towards frontal areas; planning occurs across the
parietalfrontal network (Kalaska et al. 1997).
Knowledge of arm position in space is available from
10561
Neural Representations of Intended Moement in Motor Cortex
tactile and prophoceptive information in SI, while the
location of visual cues is delivered from occipital
visual areas. There is strong evidence that the posterior
parietal cortex combines signals related to arm posi-
tion and planned arm movements, as well as for gaze
direction and location of sensory cues. (Batista and
Andersen 2001, Burnod et al. 1999). In parietal cortex
multiple frames of reference are present, although how
these are interconverted is not clear (Boussaoud and
Bremmer 1999). Further, planning for visually guided
actions begins very early in visual pathways, such as
PO, only two synapses from primary visual cortex.
Nonprimary motor areas within the frontal lobe
appear to be engaged in planning processes, based on
the observation that activity in these regions occurs
during instructed delay periods. Frontal areas are
important for linking stimuli to movements or to link
various movements together in space or time. These
more complex actions seem less coded in primary
motor cortex, where neuronal activity is more tightly
coupled to the actual performance of intended arm
movements. However, neurons related to planning
and production of motion can be found intermingled
throughout motor cortex; it appears as if only the
relative proportions change across motor areas. There
is considerable evidence that supplementary motor
cortex (SMA) is important in formulating sequences
of movements. Neurons in SMA can be selective for
particular movement sequences or transitions and
these same neurons may not be active when the same
movements are made in other sequences (Shima and
Tanji 2000). The pre-SMA, lying just in front of SMA,
appears to be critical for learning new sequences, but
the pre-SMAs role seems to fade as sequences are
learned (Hikosaka et al. 1996). The dorsal premotor
cortex PMD is also engaged in forming conditional
associations between sensory cues and movement.
While the entire PM cortex seems to be engaged in
planning in various coordinate systems, the ventricle
premotor cortex (PMv) seems to be a region for
sensorimotor processing for stimuli near the body
(Graziano and Gross 1998).
The primary motor cortex is often considered as the
final common pathway and home of the upper motor
neuron for movement commands to be issued. The
widespread origin of the corticospinal path from most
of the motor cortex coupled with the broad activation
of other motor areas during movement is sufficient to
reject these ideas in favor of a more distributed role for
motor cortex in movement. Nevertheless, the pre-
ponderance of neurons closely coupled to the details
of muscular action and the ability to activate muscles
easily with electrical stimulation from MI suggest a
special role for MI in voluntary movement. As stated
earlier, MI neurons modulate their activity with nearly
every aspect of movement including force, velocity,
acceleration, and distance. It remains a considerable
challenge to identify whether MI represents move-
ments in terms of muscle activity or more abstract
10562
variables (Todorov 2000). On the one hand, up to 5
percent of MIs output directly contacts alpha motor
neurons so that it provides a very powerful direct route
to the muscles. On the other hand, some MI neurons
are active with very abstract aspects of motor plans,
such as the serial order of stimuli, suggesting that it
participates in the cognitive events leading to action.
5. Conclusions
The combination of cortical motor areas combine
signals related to proprioceptive and tactile signals of
arm position, vision, gaze angle, attention and motor
plan, which conveys a patterned outflow of infor-
mation that guides somatic musculature for action.
The parietal lobe deals with the spatial aspects of
movement: keeping track of the configuration of the
arm in space, its relationship to the direction of gaze
and to visual cues. In addition, it participates in
formulating upcoming actions, possibly in a form
more abstract than found in the frontal lobe. The
frontal lobe motor areas contribute to learning and
assembling sequences of motor actions and are also
involved in non-spatial motor planning where ar-
bitrary cues (or perhaps thoughts) are linked to
particular motor actions. However, parietalfrontal
motor areas also combine many types of signals,
such as gaze or attention, which may have overt, or
sometimes more subtle or conditional influences upon
the activity of motor cortex neurons. Finally, this
complex of areas is nearly simultaneously engaged
in many forms of motor action so that they act in
concert when intention leads to action. The essence
of understanding how an intention becomes an action
depends on further understanding of the functional
interactions among the collection of motor areas.
See also: Classical Mechanics and Motor Control; Eye
Movement, Control of (Oculomotor Control); Motor
Control; Motor Control Models: Learning and
Performance; Motor Cortex; Motor Skills, Psy-
chology of
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J. Donoghue
Neural Representations of Objects
1. How Small Numbers of Neurons Code
Information About Objects
One of the most commonly measured units of rep-
resentation in the brain is the neuron. Somewhat
surprisingly, functional information about objects
Copyright # 2001 Elsevier Science Ltd. All rights reserved.
International Encyclopedia of the Social & Behavioral Sciences
Neural Representations of Objects
seems to be coded at this incredibly fine scale. Single-
unit recordings of neurons in the visual cortex reveal
activity that is often tuned to individual objects or
classes of objects. That is, a particular stimulus object
presented in the receptive field of a given neuron will
produce significantly greater activity (more spikes per
second) in that neuron as compared to any other tested
stimulus (typically a varied assortment of natural and
artifactual objects). For example, neurons in many
cortical extrastriate areas (the part of the primate
brain that is thought to support high-level vision,
including object recognition) in the monkey brain are
highly selective to primate faces and, sometimes, even
individual faces, and recent evidence has revealed
similar selectivity for many classes of familiar objects
(Sheinberg and Logothetis 2001). There is similar
evidence for cortical neurons specifically tuned to
individual nonface objects, at least when the stimuli
are highly familiar to the monkey (Logothetis and
Sheinberg 1996). At the same time, few researchers
believe that single neurons actually code for individual
objects. Rather, it is commonly held that large
populations of neurons represent objects or object
classes in a distributed fashion. Some evidence for this
hypothesis is provided by single-unit studies that
systematically decompose the response of a given
neuron by exploring which particular features of an
object are actually driving neural activity. It is often
the case that the maximum response is maintained
when only schematic elements of the object are
presented, suggesting that single neurons must work in
concert to represent an object (Tanaka 1996).
To the extent that individual neurons participate in
the representation of a given object, there remains the
question of the format of this representation (Marr
1982). Object representations can be more or less
invariant over changes in the appearance of the object
in the image (see Object Recognition: Theories). Ideal-
ly, perception and recognition should remain robust
when an object is moved, rotated, or illuminated
differently. Most object-tuned neurons exhibit some
invariance: the level of response to a preferred object is
not dramatically affected by changes in the size or the
spatial position of an object for which a given neuron
is selective. On the other hand, these same neurons
often show great sensitivity to changes in orientation,
viewpoint, and illumination direction. For example, a
large percentage of object-tuned neurons are also
view-tuned in that they show the highest level of
activity to specific objects in specific viewpoints. Face-
selective neurons may respond most strongly when
presented with a frontal view of a face, but show a
progressively diminished response as the face rotates
away from this viewpoint. Similarly, in the visual
cortex of monkeys taught to recognize novel objects,
neurons that become selective for these objects are
typically highly tuned to the particular viewpoints
used during training. These findings are consistent
with much of the behavioral data on object recogni-
10563
ISBN: 0-08-043076-7