Download The organization of the cortical motor system: new concepts

Electroencephalography and clinical Neurophysiology 106 (1998) 283–296
Invited review
The organization of the cortical motor system: new concepts
G. Rizzolatti*, G. Luppino, M. Matelli
Istituto di Fisiologia Umana, Università di Parma, via Gramsci 14, I-43100 Parma, Italy
Abstract
A series of recent anatomical and functional data has radically changed our view on the organization of the motor cortex in primates. In
the present article we present this view and discuss its fundamental principles. The basic principles are the following: (a) the motor cortex,
defined as the agranular frontal cortex, is formed by a mosaic of separate areas, each of which contains an independent body movement
representation, (b) each motor area plays a specific role in motor control, based on the specificity of its cortical afferents and descending
projections, (c) in analogy to the motor cortex, the posterior parietal cortex is formed by a multiplicity of areas, each of which is involved in
the analysis of particular aspects of sensory information. There are no such things as multipurpose areas for space or body schema and (d)
the parieto-frontal connections form a series of segregated anatomical circuits devoted to specific sensorimotor transformations. These
circuits transform sensory information into action. They represent the basic functional units of the motor system. Although these conclusions mostly derive from monkey experiments, anatomical and brain-imaging evidence suggest that the organization of human motor cortex
is based on the same principles. Possible homologies between the motor cortices of humans and non-human primates are discussed.  1998
Elsevier Science Ireland Ltd.
Keywords: Motor cortex; Premotor areas; Parietal lobe; Parieto-frontal connections
1. Introduction
The view on motor cortex organization that dominated
the second half of this century was rather simple. Roughly,
it was the following. In the posterior part of the frontal lobe
there are two complete representations of body movements
(Penfield and Welch, 1951; Woolsey et al., 1952). The first
is located on the lateral cortical convexity, the other lies on
the mesial cortical surface. The first representation is large
and detailed. It includes the whole of area 4 and most of
lateral area 6. This representation is the ‘primary motor
cortex’ or M1. The second representation is located on the
cortical mesial surface. It is smaller than the former, less
precise and with an emphasis on proximo-axial movements.
This representation is the supplementary motor area (SMA,
Penfield and Welch, 1951; Woolsey et al., 1952).
This extremely simple (one may say even simplistic)
view of cortical motor organization has changed radically
in the last years. New and more refined anatomical and
functional techniques have shown, first in non-human pri* Corresponding author. Tel.: +39 521 290380; fax: +39 521 291304;
e-mail: [email protected]
0013-4694/98/$19.00  1998 Elsevier Science Ireland Ltd. All rights reserved
PII S0013-4694 (98 )0 0022-4
mates and, more recently, (and with much less detail) in
humans, that cortical motor organization is much more
complex than thought previously. Among the new aspects
of motor organization some are particularly important. We
list them straight away, at the onset of this review, in order
to make it clear its logic.
(1) The motor cortex (defined as the agranular sector of
the frontal lobe) is formed by a mosaic of anatomically and
functionally distinct areas. The classical view that there are
only two motor areas is wrong. (2) Like the motor cortex,
the posterior parietal lobe is constituted by a multiplicity of
areas with distinct anatomical and functional properties.
Each parietal area is involved in the analysis of particular
aspects of sensory information. There is no such a thing as a
multipurpose area for perception of space or body schema.
(3) Motor and parietal areas are reciprocally connected and
form a series of specialized circuits working in parallel.
These circuits transform sensory information into action.
They are the basic elements of the motor system.
The aim of this article is to present this new picture of the
organization of the cortical motor system and to discuss the
possible functions of the various parieto-frontal circuits.
Although most of the reviewed data concern non-human
EEG 98538
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primates, the available data on human cortical organization
confirm the general validity of the picture presented here.
1990). In contrast, it has no connections with other motor
(skeletomotor) fields.
2. The motor areas of the frontal lobe
3. The general organization of the posterior parietal
cortex
A modern parcellation of the agranular frontal cortex
(motor cortex) of the macaque monkey is shown in Fig. 1.
The subdivision is based on cytoarchitectural and histochemical data (Matelli et al., 1985, 1991). F1 basically corresponds to area 4 of Brodmann (1909), the other areas are
subdivsions of Brodmann’s area 6. F2 and F7, which lie in
the superior part of area 6, are often referred to collectively
as ‘dorsal premotor cortex’, while F4 and F5, which lie in
the inferior area 6, are often referred to as ‘ventral premotor
cortex’. F3 and F6 form the mesial area 6. (For a review of
the various parcellations of the motor cortex, see Wise et al.,
1991; Matelli and Luppino, 1996).
The validity of the anatomical subdivision shown in Fig.
1 is confirmed by functional data. Single-neuron recordings
and intracortical microstimulation (see below) have demonstrated that the motor cortex contains many functional
motor representations (motor fields). These motor representations are located in different anatomical areas and not in
two, as classically believed. Their location is shown in Fig.
1. The motor representation of F7 is not fully established. It
is known, however, that its dorsal part is devoted to the
control of eye movements (supplementary eye field, SEF,
Schlag and Schlag-Rey, 1987).
The multiplicity of motor fields presented in Fig. 1 is in
good accord with recent studies of corticospinal projections
(He et al., 1993, 1995). Following injections of retrograde
neural tracers into the cervical segments, marked neurons
were found in the arm fields of F1, F2, F3, F4 and F5. When
injections were made into the lumbar segments of the spinal
cord, labeling was found in the leg fields of F1, F2 and F3.
Among the frontal motor areas, two – F6 and F7 – are
virtually devoid of corticospinal neurons. Their main descending projections terminate in the brain stem (Keizer and
Kuypers, 1989).
The connections among the various motor areas show a
pattern consistent with the organization of corticospinal projections. The two areas that do not send corticospinal projections (F6 and F7) do not send projections to F1 either,
being connected only with the motor areas located rostral to
F1 (F2, F3, F4 and F5) (Barbas and Pandya, 1987; Luppino
et al., 1993). Conversely, F6 and F7 receive a strong input
from the prefrontal cortex, a finding suggesting that they
represent the main entrance of the prefrontal input to the
motor cortex (Barbas and Pandya, 1987; Luppino et al.,
1993; Lu et al., 1994). All motor areas rostral to F1 are
linked one with another. Their connections, however, are
not random, but selectively link fields with similar functions
(Dum and Strick, 1991b; Luppino et al., 1993). Finally, the
eye movement representation in F7 is strongly connected to
the frontal eye fields (Huerta and Kaas, 1990; Luppino et al.,
Anatomically, the posterior parietal cortex is formed by
two lobules: the superior parietal lobule (SPL) and the inferior parietal lobule (IPL). The areas forming the posterior
parietal cortex are shown in Fig. 1.
An important finding that emerges from recent anatomical and functional experiments is that in the posterior parietal lobe, as in the motor cortex, there is multiplicity of
arm, leg and face representations. In particular, the arm
(the skeletomotor representation best studied) is represented
at least 8 times (see Fig. 1).
For a long time it was believed that IPL is related to both
visual and somatosensory information, while SPL is exclusively related to the somatosensory one. Recent data have
shown that this picture is incorrect. There is now evidence
that both lobules receive somatosensory and visual inputs.
The modern view is that the posterior areas of both SPL and
IPL process predominantly visual information, whereas the
anterior areas are related to somatosensory modality in SPL
and to an integration of somatosensory and visual information in IPL (for a review of the literature, see Caminiti et al.,
1996; Rizzolatti et al., 1997b; Wise et al., 1997).
4. Parieto-frontal circuits: organizational principles
The parieto-frontal circuits represent the basic elements
of the cortical motor system. The general pattern of these
circuits is the following. Each motor area receives afferents
from a specific set of parietal areas. The input from one area
is rich (‘predominant’ input), while that from the other areas
is moderate or weak (‘additional’ inputs). In turn, each parietal area is connected with several motor areas, but has
privileged contacts with one only. Exceptions to this are
area PFG, which sends an approximately equal amount of
fibers to several motor areas, and V6A which projects to two
of them. Parietal and frontal areas linked by a ‘predominant’
connection have similar functional properties, whereas this
similarity is not so obvious if one compares the functional
properties of areas linked by ‘additional’ connections.
If one takes into account the ‘predominant’ connections
between parietal and motor areas, a series of segregated
parieto-frontal functional circuits can be distinguished.
Each circuit is involved in a specific sensory-motor transformation for action and, thus, represents the functional unit
of the cortical motor system (see Rizzolatti et al., 1997b).
Table 1 lists the ‘predominant’ and ‘additional’ afferents
from SPL and IPL of each motor area and their other, most
important, postrolandic connections. Parieto-prefrontal circuits are not shown in the table, because they are outside the
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Fig. 1. Mesial and lateral views of the macaque brain showing the cytoarchitectonic parcellation of the agranular frontal cortex and of the posterior parietal
cortex. Motor areas are defined according to Matelli et al. (1985, 1991). The terminology used derives from that used by von Economo for the human cortex
that indicates all the frontal areas, including the motor ones, with the letter F. At variance with von Economo, numbers, instead of letters, identify the various
areas. All parietal areas except those buried within the intraparietal sulcus are defined according to Pandya and Seltzer (1982). The areas located within the
intraparietal sulcus (IP) are defined according to physiological data (for references see text) and are shown in an unfolded view of the sulcus in the lowest part
of the figure. On the basis of the available data, the various body-parts representations are reported. In the prefrontal cortex the frontal eye field (FEF) is also
defined according to physiological criteria. The superior arcuate sulcus (AS), the inferior arcuate sulcus (AI) and the inferior precentral dimple are drawn in
blue, red and green, respectively. The suggested homologues of these sulci in the human brain are drawn with the same colors in Fig. 3. AG, annectant gyrus;
C, central sulcus; Ca, calcarine fissure; Cg, cingulate sulcus; IO, inferior occipital sulcus; L, lateral fissure; Lu, lunate sulcus; OT, occipitotemporal sulcus; P,
principal sulcus; POs, parieto-occipital sulcus; ST, superior temporal sulcus.
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Table 1
Parieto-frontal projections in the macaque monkey
Motor areas
Posterior parietal areas
Predominant
connections
F1
F2 – dimple region
F2 – ventrorostral
F3
F4
F5 – convexity
F5 – bank
F6
F7
F7-SEF
PE
PEc-PEip
MIP
PEci
VIP
PF
AIP
PGm
Other postrolandic
areas
Additional
connections
PFG
V6A-PFG
PE-PFG
PF-PEip
AIP
PFG
PFG
V6A-PG
LIP
SI
CGp
CGp
SII-SI
SII
SII
SII
CGp
scope of the present article. Fig. 2 shows the ‘predominant’
connections between the posterior parietal areas and the
motor areas.
5. PE-F1 circuit
It is a classical notion that area PE (area 5) is a higherorder somatosensory area mostly devoted to the analysis of
proprioceptive information. The most effective stimuli for
many PE neurons are specific combinations of multiple joint
positions or combinations of joint and skin stimuli (Sakata
et al., 1973; Mountcastle et al., 1975). Recently, Lacquaniti
et al. (1995) provided evidence that many neurons in area
PE encode the location of the arm in space in a body-centered coordinate system. The main role of PE-F1 (M1) circuits (Fig. 2A) appears to be that of providing F1 with
information on the location of body parts necessary for
the control of movement of limbs and other body parts.
The notion that PE-F1 is a skeletomotor circuit is supported
by anatomical data showing that, in contrast to the posterior
SPL areas, PE does not receive visual inputs (see Caminiti et
al., 1996).
In addition to input from PE, F1 receives connections
from motor areas F2, F3, F4 and F5. F1 is the area that
plays a major role in segmenting actions planned by other
motor areas into elementary movements, and is virtually
unique among the motor areas in controlling independent
finger movements (see Porter and Lemon, 1993).
6. Inferior area 6 (‘ventral premotor cortex’) circuits
The inferior sector of Brodmann area 6 is constituted by
two distinct areas: F4 and F5 (Matelli et al., 1985). Recent
cytoarchitectonic and immunohistochemical findings have
shown that area F5 is not homogeneous but is formed by two
major sectors (Matelli et al., 1996). One is located on the
posterior bank of the inferior arcuate sulcus (F5 of the arc-
uate bank, F5ab), the other is located on the cortical convexity immediately adjacent to the arcuate sulcus (F5 of the
cortical convexity, F5c). Functional data confirm this morphological subdivision. Each of the 3 subdivisions of inferior area 6 is part of a different parieto-frontal circuit. The
properties of the 3 circuits will be dealt with separately in
the sections below.
6.1. The VIP-F4 circuit
Area VIP occupies the fundus of the intraparietal sulcus
(Fig. 2B; Colby et al., 1993). It receives visual projections
from various areas belonging to the ‘dorsal visual stream’
(among them areas MST and MT) that are involved in the
analysis of optic flow and motion (Maunsell and Van Essen,
1983; Ungerleider and Desimone, 1986; Boussaoud et al.,
1990). In addition, VIP receives somatosensory information
from areas PEc and PFG (Seltzer and Pandya, 1986).
VIP neurons fall into two main categories: purely visual
neurons and bimodal, visual and tactile, neurons (Colby et
al., 1993; Bremmer et al., 1997). Purely visual neurons are
often selective for expanding or contracting visual stimuli.
Others are strongly selective for the direction and speed of
stimuli moving along the sagittal plane. Bimodal neurons
respond independently to visual and tactile stimuli. Their
tactile receptive fields (RFs) are located predominantly on
the face. Their visual RFs are located in parts of the field of
vision corresponding to the tactile RFs (e.g. tactile RF on
the right side of the upper face, visual RF in the right upper
quadrant of the visual field). Many neurons respond to
visual stimuli only when they are located in the space
around the body (peripersonal space). In about one third
of visually-responsive neurons, the visual RF is encoded
in egocentric and not in retinal coordinates (Bremmer et
al., 1996). That is, regardless of where the gaze is directed,
the visual RF remains in the same location with respect to
the body.
The main target of area VIP in the frontal lobe is area F4
(Fig. 2B; Matelli et al., 1994). Microstimulation experiments have shown that in F4, arm, neck, face and mouth
movements are represented (Gentilucci et al., 1988). Arm
and axial movements are located medially in F4, oro-facial
movements more laterally. Single neuron recordings confirmed the existence of these various representations (Godschalk et al., 1981; Gentilucci et al., 1988). They showed
also that many neurons fire during reaching movements
directed toward the body or away from it. Others discharge
during oro-facial movements. Neurons related to distal
movements are virtually absent.
As in area VIP, F4 neurons can be subdivided into two
categories according to their responses to sensory stimuli:
bimodal neurons (56%) and unimodal neurons (44%;
Fogassi et al., 1996). However, in contrast to VIP, unimodal
neurons are typically tactile, purely visual neurons being
very rare. Unimodal and bimodal neurons have the same
somatosensory characteristics. Their RFs are rather large
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Fig. 2. Summary view of the main posterior parietal projections to the motor cortex in the macaque monkey (see also Table 1). (A) Parietal projections from
areas located in the superior parietal lobule. In this view of the brain the inferior parietal lobule and the occipital lobe have been removed, in order to show the
areas located in the medial bank of the intraparietal sulcus and in the anterior bank of the parieto-occipital sulcus, respectively. (B) Parietal projections from
areas located in the lateral bank and in the fundus of the intraparietal sulcus. In order to show these areas, the intraparietal sulcus has been opened and the
occipital lobe removed. Dashed line marks the fundus of the sulcus. (C) Parietal projections from areas located on the convexity of the inferior parietal lobule.
Abbreviations as in Fig. 1.
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and predominantly located on the face, arm and the upper
part of the body. The visual RFs are located in the peripersonal space, in register with the tactile fields. In most cases,
the visually-responsive neurons respond preferentially to
stimuli directed toward the tactile RF. In a large majority
of these neurons (70%) the position of the visual RF does
not change when the gaze moves. Similarly, the visual RF
remains anchored to the tactile RF when the body part, on
which the tactile RF is located, is moved. Taken together,
these properties indicate that in F4 the space is encoded in
body-parts-centered coordinates (Graziano et al., 1994;
Fogassi et al., 1996). They indicate also that there is no
single reference point (head, arm or body midline), but,
rather, there is a multiplicity of reference points depending
on the type of movement encoded by a given set of neurons
(Graziano et al., 1997; Rizzolatti et al., 1997a).
In conclusion, the functional properties of VIP-F4 circuit
indicate that this circuit plays a role in encoding the peripersonal space and in transforming object locations into
appropriate movements toward them.
6.2. The AIP-F5ab circuit
Area AIP occupies the rostral part of the lateral bank of
the intraparietal sulcus (IPs) in front of area LIP (Fig. 2B).
Neurons of this area were studied in monkeys trained to
reach and grasp objects of different sizes and shapes. The
testing was carried out both in darkness and in light. The
results showed that most of them discharge during grasping
of specific objects. Their activity is not influenced by object
position in space, a finding showing that their discharge is
indeed related to hand and finger movements and not to
proximal arm movements (Taira et al., 1990; Sakata et al.,
1995).
AIP neurons were classified into 3 groups: ‘motor-dominant’, ‘visual and motor’ and ‘visual-dominant’ neurons.
‘Motor-dominant’ neurons do not show any significant difference in activity when tested in darkness or light, ‘visual
and motor’ neurons are less active in darkness than in light,
‘visual-dominant’ neurons fire vigorously only when the
stimulus is visible. Many visually-responsive neurons
were found to discharge also during fixation of the objects,
even when fixation was not followed by a subsequent grasping movement. Finally, in most ‘visual and motor’ neurons,
the intrinsic characteristic of the object, effective in triggering a neuron and the type of grip encoded by that neuron,
coincided (Taira et al., 1990; Sakata et al., 1995).
Area AIP is richly connected with motor area F5ab where
distal arm movements are also represented (Fig. 2B; Matelli
et al., 1994). F5 neurons discharge during specific goaldirected actions performed with the hand, the mouth or
both. According to the action effective in triggering them,
F5ab neurons were subdivided into various classes. Among
them, the most represented are: grasping, holding, tearing
and manipulating neurons. Most ‘grasping’ neurons code
specific types of hand prehension, such as for example,
precision grip, whole-hand prehension, finger prehension.
The temporal relation of neuron discharge with hand movements changes from neuron to neuron. Some neurons fire
during the last part of grasping, others start to fire with
finger aperture and continue during finger closure, others
are activated in advance of the onset of finger movements
(Rizzolatti et al., 1988).
Similarly to AIP neurons, many F5ab neurons discharge
to the presentation of 3D objects, even when no immediate
or subsequent action upon the object is allowed (Murata et
al., 1997). Recent PET data indicate that a similar activation
of area 6 occurs also in humans at the presentation of graspable objects such as, for example, tools of common usage
(Grafton et al., 1997).
Taken together, the AIP-F5ab data suggest that this circuit plays a crucial role in transforming the intrinsic properties of the object into the appropriate hand movements
(Jeannerod et al., 1995). The description of object characteristics, possibly in terms of their affordances, is carried out
in AIP and then is transmitted to F5ab, where different types
of grips are encoded. The matching between object description and type of grip allows the selection of the grip effective for a given object (Gallese et al., 1997). A formal model
of object to grasp transformation was provided by M.A.
Arbib and A.H. Fagg (unpublished data).
Strong support for a crucial role of AIP-F5ab in visuomotor transformation for grasping movements was recently
offered by studies in which the two areas were separately
inactivated (Gallese et al., 1994, 1997). The main effect
observed following independent inactivation of AIP and
F5ab was a disruption of the preshaping of the hand during
grasping. The deficit consisted in a mismatch between the
features of the object that had to be grasped and the posturing of finger movements. When the monkey was successful
in grasping the objects, the grip was achieved only after a
series of corrections that relied on tactile exploration of the
object. These data clearly show that lesion of the AIP-F5ab
circuit does not disrupt the ability to perform grasping
movements, but only the capacity to transform the 3D properties of the object into appropriate hand movements.
6.3. The PF-F5c circuit
Neurons located in F5c are indistinguishable from F5ab
neurons as far as their motor properties are concerned. Like
those neurons, they discharge during specific goal-directed
actions. The visual properties, however, of F5ab neurons are
markedly different from those of F5c. Their main characteristic is that they discharge when the monkey observes
another individual performing an action similar to that
encoded by the neuron. Object presentation is not sufficient
to activate them. Because of this correspondence between
visual and motor properties, these neurons were called ‘mirror neurons’ (Gallese et al., 1996; Rizzolatti et al., 1996a).
The observed actions that most commonly activate the
mirror neurons are: grasping, placing and manipulating
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objects. Most of them respond selectively when the monkey
watches only one type of action (e.g. grasping). Others fire
in response to two or more actions (e.g. grasping and placing).
Typically, mirror neurons show congruence between the
observed and the executed action. This congruence can be
very strict, that is the effective motor action (e.g. precision
grip) coincides with the action that, when seen, triggers the
neuron (e.g. precision grip). For others the congruence is
broader. For these neurons, the motor requirements to trigger them (e. g. precision grip) are usually stricter than the
visual ones (e.g. any type of hand grasping).
Tracer injections in F5c showed that its predominant
inputs come from area PF (Fig. 2C). Neurons with mirror
characteristics are certainly present in PF, but their properties have not been yet studied in details (our unpublished
data).
The discovery of mirror neurons is very important
because it suggests an important cognitive role for the
motor cortex: that of representing actions internally. This
internal representation, when evoked by an action made by
others, should be involved in two related functions: action
imitation and action recognition. It is outside the scope of
the present review to discuss in detail the data and the theoretical considerations on which this hypothesis is based
(Rizzolatti et al., 1996a; Rizzolatti and Arbib, 1998). It is
of interest here to stress, however, that an observation/
execution matching system, similar to that just described,
is present also in humans.
Transcranial magnetic stimulation (Fadiga et al., 1995),
PET experiments (Rizzolatti et al., 1996b) and more
recently MEG data (Hari et al., unpublished data) all indicate that the mere observation of an action activates the
motor system of the observing individual. This activation
includes, in addition to the region of the left superior temporal sulcus (where in the monkey neurons encoding biological motion are located), the left inferior parietal lobe,
Broca’s area and the precentral cortex.
7. Superior area 6 (‘dorsal premotor’) circuits
Superior area 6 is constituted by two areas: F2 and F7
(Fig. 1). F2 appears to be cytoarchitectonically homogeneous. Recent evidence suggests, however, that, it should
be subdivided into two functional sectors: one located
around the superior frontal dimple, the other occupying its
ventrorostral part (Raos et al., unpublished data). The two
F2 sectors receive (with some overlap) different parietal
inputs (Matelli et al., unpublished data). The sector around
the dimple is the target of areas PEc and PEip, while the
ventrorostral receives its predominant input from area MIP
(Fig. 2A).
Like F2, F7 also consists of two distinct functional sectors: a medial one and a lateral one. The medial sector
corresponds to the supplementary eye field of Schlag and
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Schlag-Rey (1987). This sector receives its main parietal
input from area LIP (Huerta and Kaas, 1990). LIP-F7
(SEF) is a circuit involved essentially in the control of eye
movements. The lateral sector receives its main input from
PGm (Fig. 2A; Matelli et al., unpublished data).
7.1. The PEc/PEip-F2 dimple and MIP-F2 ventrorostral
circuits
In several studies, neurons were recorded from the rostral
part of the medial bank of the intraparietal sulcus (basically
area PEip). The results have shown that most of them
respond to somatosensory stimuli (Mountcastle et al.,
1975; Iwamura and Tanaka, 1996). Many become active
in association with arm movements (Kalaska et al., 1990).
Typically, the discharge is stronger when the arm is projected in a certain direction. The directional tuning is
usually broad.
In a recent experiment, neurons with very intriguing
properties were described in the medial bank of the intraparietal sulcus, most probably in the posterior part of area
PEip. These neurons had bimodal, tactile and visual RFs
(Iriki et al., 1996). The tactile RFs were located on the
arm. The visual RFs extended in the space around the tactile
RFs. The most interesting finding was that the visual RFs
were not fixed in their extension, but expanded when the
monkey prepared for a specific motor action. The functional
properties of these neurons are, in many aspects, similar to
those of F4 neurons, but not to those found in the F2 dimple
region (see below). Given that PEip sends ‘additional’ projections to F4, it is possible that this set of neurons projects
to F4 rather than to the area target of PEip ‘predominant’
output (see Fig. 2A).
As far as we know, there are no specific physiological
studies devoted to the functional properties of area PEc.
This area is richly connected with area PE (Pandya and
Seltzer, 1982). It is likely, therefore, that area PEc, like
PE, is involved in the analysis of somatosensory stimuli
for movement organization. Electrophysiological studies
of neighboring regions, in which PEc neurons were occasionally recorded, confirm this conclusion (Colby and
Duhamel, 1991; Galletti et al., 1996).
While PEip and PEc appear to be mostly involved in
somatosensory control of movements, both area MIP
(Colby et al., 1988) and area V6A (Galletti et al., 1996)
also use visual information for the same purpose.
Neurons responding both to visual and somatosensory
stimulation were frequently recorded in MIP (Colby and
Duhamel, 1991). Detailed information on the functional
properties of this area, however, is lacking. More data are
available on area V6A. This area represents the dorsal part
of the region originally described as area PO (Gattass et al.,
1985). About half of V6A neurons discharge in response to
visual stimuli. The remainders discharge mostly in association with eye or arm movements (Galletti et al., 1996, 1997).
In contrast to what is observed in most visual areas, in V6A
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there is no magnification of the foveal representation (Colby
et al, 1988; Gattass et al., 1997).
All 4 parietal areas described in this section project to
area F2. As mentioned above, however, their connection
pattern is not the same: areas PEip and PEc project mostly
to the dimple region of F2, whereas areas MIP and V6A
project to the ventrorostral F2 (Fig. 2A).
The dimple region of F2 is somatotopically organized. Leg
movements are represented dorsal to the dimple, while arm
movements are located ventral to it (Kurata, 1989; Dum and
Strick, 1991a; He et al., 1993; Godschalk et al., 1995). Some
anatomical evidence suggests that, within the dimple, there is
also a representation of distal arm movements (He et al.,
1993). Functional studies of F2 were mostly focused on the
motor properties of its neurons. They showed that some F2
neurons discharge in association with movement onset, while
others become active long in advance of it. It is likely that
neurons showing this anticipatory discharge play a role in
motor preparation (see Kurata, 1994; Wise et al., 1997).
Some neurons respond to the presentation of visual stimuli
instructing the monkey on the movement that they have subsequently to perform. The percentage of these ‘signal-related’
neurons is higher in the rostral part of F2 than in its caudal part
(dimple region) (Tanné et al., 1995; Caminiti et al., 1996;
Johnson et al., 1996).
There is little information on the responses of F2 neurons
to sensory stimuli. Preliminary observations from our
laboratory indicate that there is a differential distribution
of sensory properties within F2. While in the dimple region
most neurons respond to proprioceptive stimuli, in ventrorostral F2 neurons respond also to tactile and visual stimulation (Raos et al., unpublished data). This functional segregation of sensory modalities within F2 is consistent with
the parietal input to the two F2 subregions.
In conclusion, the PEip/PEc-F2 dimple circuit appears to
be involved in planning and controlling arm (and leg) movements on the basis of somatosensory information. In contrast, the MIP/V6A-F2 ventrorostral circuit uses somatosensory and visual information, probably for the same purpose. Monitoring and controlling arm position during the
transport phase of the hand toward the target could be one of
the major functions of this circuit. The optic ataxia symptoms that typically result as a consequence of damage to
superior parietal lobule (De Renzi, 1982; Milner and Goodale, 1995), fit this hypothesis well.
7.2. The PGm-F7 circuit
Area PGm is cytoarchitecturally similar to area PG (Pandya and Seltzer, 1982). It is richly connected with this area
and with V6A (Pandya and Seltzer, 1982; Colby et al., 1988;
Cavada and Goldman-Rakic, 1989; Andersen et al., 1990).
PGm neurons discharge during eye and/or arm movements
(Ferraina et al., 1997a,b). The functional role of this complex area is largely unknown. Area PGm is the major source
of parietal input to lateral F7 (Fig. 2A).
Recording studies have shown that in F7 there are neurons that discharge in relation to arm movements, others that
fire before movement onset, and others active in response to
visual stimuli. Visually-responsive neurons are more
numerous in F7 than in F2. Furthermore, unlike in F2,
visually-responsive F7 neurons do not require a subsequent,
stimulus-related, movement to become active (di Pellegrino
and Wise, 1991).
Vaadia et al. (1986) tested F7 neurons in a behavioral
paradigm in which reaching movements were: (a) triggered
by and directed toward the same visual (or acoustical)
source, or (b) triggered by a given sensory source, but directed to a spatial position different from that of this source.
They found that some F7 neurons fired exclusively in the
first condition. They proposed that these neurons contribute
to spatial localization of external stimuli for reaching movements.
A further function of area F7 is that this area, possibly
with the contribution of F2, plays a crucial role in conditional stimulus-response association tasks (see Passingham,
1993). Evidence in favor of this hypothesis derives from
ablation studies carried out by Halsband and Passingham
(1982) and Petrides (1982). Halsband and Passingham
(1982) ablated the postarcuate cortex along the superior
and inferior branches of the arcuate sulcus in monkeys previously trained to make arbitrary goal-directed movements
in response to colored stimuli. After the lesion, the monkeys
were unable to execute the task any longer, although no
obvious motor deficit was present. Similar results were
obtained by Petrides (1982) following ablation of the
periarcuate cortex in monkeys which also had previously
learned a conditional association motor task. If one compares the lesions made by the two groups of researchers,
it appears that F7 and the rostralmost part of F2 were the
only regions damaged in all monkeys. Thus, F7, possibly
with a contribution of F2, appears to play an important
role in conditional movement selection. Lesion studies
in patients suggest a similar role for the dorsal premotor
cortex of humans (Petrides, 1985; Halsband and Freund,
1990).
8. Mesial area 6 circuits
Mesial area 6 was classically considered to be a single
area: the supplementary motor area (Penfield and Welch,
1951; Woolsey et al., 1952). Recent cytoarchitectural, histochemical, and functional data have clearly shown that in
the monkey the mesial surface of area 6 is occupied by two
areas: F3 or SMA proper and F6 or pre-SMA (Luppino et
al., 1991; Matelli et al., 1991). F3 receives its main parietal
input from area PEci (Fig. 2A; Luppino et al., 1993). F6 is
the only motor area that cannot be considered part of a
specific parieto-frontal circuit. While it receives a very
strong input from the prefrontal lobe, it has very little
input from the parietal lobe (Luppino et al., 1993).
G. Rizzolatti et al. / Electroencephalography and clinical Neurophysiology 106 (1998) 283–296
291
8.1. The PEci-F3 circuit
8.2. Prefrontal lobe/F6 (pre-SMA) circuit
Area PEci was defined by Pandya and Seltzer (1982) as a
parietal area localized in the caudal part of the cingulate
sulcus (Fig. 1). Anatomical data from the same authors
showed that area PEci is connected with areas PE, PEc
and PGm. There is only one functional study of this area
(Murray and Coulter, 1981). This study showed that in PEci
there is a complete somatosensory map of the body. Because
of this finding and its anatomical location, PEci was named
the ‘supplementary sensory area’.
PEci is the main source of input to area F3. Additional
inputs to the latter area come from areas 23, SII and, to
lesser extent, SI, PE and PFG (Luppino et al., 1993). F3
contains a complete somatotopic representation of body
movements (Mitz and Wise, 1987; Luppino et al., 1991).
The leg field is located caudally, the arm field rostrally. The
arm and leg fields form two oblique bands running from a
ventro-caudal to a dorso-rostral location. The face field,
much smaller than the other two, is located at the rostral
end of the arm field.
Single-neuron recordings showed that many F3 neurons
(in the case of studies preceding the subdivision of SMA
in F3 and F6, neurons located in the caudal part of SMA)
respond to somatosensory stimuli, few to visual stimuli
(see Tanji and Shima, 1994; Rizzolatti et al., 1996c).
Most F3 neurons discharge in association with active movements. Although the relation between the discharge and
movement may vary greatly from one neuron to another,
the discharge onset of F3 neurons is typically time-locked
to the movement onset. Some neurons fire exclusively in
relation to specific sequences of movements (Tanji et al.,
1996).
The behavior of F3 neurons is, for many aspects, similar
to that of F1 (area 4) neurons. There are, however, some
organization properties that distinguish the two areas: (a) in
F1 proximal and distal movement are anatomically segregated, while they are mixed in F3, (b) intracortical electrical
microstimulation evokes body part movements around a
single joint in F1, whereas movements involving two or
more articulations are often observed in F3 (Mitz and
Wise, 1987; Luppino et al., 1991) and (c) although there
is some controversy on this point (see He et al., 1995), most
authors agree that in F3 proximal movements are much
more represented than distal movements (Penfield and
Welch, 1951; Woolsey et al., 1952; Luppino et al., 1991;
Matelli et al., 1993; Maier et al., 1997; Rao et al., 1997)
whereas this is not the case for F1.
Taken together, these data suggest that the PEci-F3 circuit controls motor activity in a global way. A more specific
interpretation of the possible functional role of F3 role in
motor control was advanced by Massion and his co-workers
(Massion, 1992). Their view, based on patients’ data, is that
F3 plays an important role in the control of posture and, in
particular, in the postural adjustments that precede voluntary movements.
At variance with all other motor areas, the input that F6
(pre-SMA) receives from the parietal lobe is very modest. In
contrast, it receives a substantial input from area 46 and
from the rostral cingulate cortex (area 24c; Luppino et al.,
1993; Lu et al., 1994). This peculiar anatomical organization suggests that F6, unlike the other motor areas, is
involved in a control of motor processing of the parietofrontal circuits, rather than in sensorimotor transformations
for action execution.
A large body of data, coming both from brain-imaging
studies in humans, and neuron-recording data in monkeys, is
consistent with this ‘supramotor’ function of F6. Anatomical and neurochemical data have shown that in humans (as
in monkeys) the border between pre-SMA and F3 (SMA
proper) corresponds to a frontal plane passing through the
anterior commissure (Zilles et al., 1995). Thus, activations
observed in human brain-imaging studies anterior to this
plane indicate activations of pre-SMA, while activations
posterior to it indicate activity of SMA proper. Using this
localization criterion and correlating the activation site with
the examined task, it is clear that while SMA proper is
activated by ‘simple’ movements, pre-SMA requires ‘complex’ motor acts in order to be activated (Deiber et al., 1991;
Matelli et al., 1993; see, for review, Picard and Strick,
1996).
The expressions ‘simple’ and ‘complex’ movements are,
of course, vague terms that certainly do not define with
precision the functional role of pre-SMA. A possible clue
as to what may be the key factor for activating pre-SMA
comes from monkey studies. Recording of F6 neurons in a
natural situation showed that, unlike F4 and F5 neurons, F6
neurons do not discharge in association with distal and proximal arm movements, but control actions globally. Some
neurons discharge at visual presentation of graspable
objects independently of their location, but increase their
firing as the stimulus is moved toward the monkey. Others,
on the contrary, are inhibited at the presentation of the
graspable object, but start to discharge as soon as it is
being brought close to the monkey. There are several facilitation/inhibition combinations that characterize different
F6 neurons. What appears to be constant, however, is the
modulation of the neuron’s discharge according to whether
an object can or cannot be grasped (Rizzolatti et al.,
1990).
The interpretation of these findings that we favor, is that
F6 neurons constitute a system that controls the potential
actions encoded in the lateral parieto-frontal circuits. Normally, even when the neurons encoding these potential
actions are activated, movement does not start. Only when
external contingencies and motivational factors allow it, the
control system represented by F6 (and possibly by the rostral motor cingulate area 24c) renders the onset of movement possible. The degree of activity in F6 depends, in turn,
on the behavioral situation in which the stimulus is (close-
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G. Rizzolatti et al. / Electroencephalography and clinical Neurophysiology 106 (1998) 283–296
distant, presence of obstacle, physical possibility to act) and
on motivation.
This hypothesis is not in contrast with the notion that preSMA may plays an important role in sequence organization
(Tanji et al., 1996). It put the emphasis, however, not on
sequence per se, but on the particular interplay of facilitation and inhibition that motor sequences, especially when
complex, require.
9. Possible homologies between human and monkey
motor cortex
The new view on cortical motor organization that we
presented in the previous sections is in large part based on
monkey data. While it is immediately apparent from brain
gross anatomy and cytoarchitectonic data that human cortical organization is similar (although obviously of much
greater complexity) to that of the monkey, nevertheless it
is not easy to transfer data from monkey circuits to human
circuits, first, because precise homologies between monkey
and human cortical areas are difficult to establish and second, because even with the most advanced brain-imaging
technique developed in the last decade, the degree of detail
that one can obtain in human experiments is incomparably
lower than that obtainable in primate experiments.
In spite of these limitations, it is of interest to draw a
comparison between human and monkey motor cortices in
order to have a starting point for testing functional hypotheses derived from monkey experiments in human subjects,
and for better understanding, therefore, human motor cortex
organization.
Fig. 3A shows a lateral view of human frontal lobe, in
which the cytoarchitectonic parcellation of the motor cortex
(Vogt and Vogt, 1919) and the motor representations, as
determined by electrical surface stimulation (Foerster,
1936), are presented. There are 3 aspects of this map that
are worth noting. (a) The surface of the precentral gyrus
belongs mostly to area 6aa and not to area 4 (as frequently
believed). Area 4 is buried for most of its extent in the
central sulcus. This location of area 4 is in agreement
with modern data on this issue (Geyer et al., 1996; see
also Preuss et al., 1996). (b) An ordered movement representation is present in area 6aa (Foerster, 1936). This
further motor representation on the lateral brain surface
indicates that motor representation is multiple in humans
as in monkeys (see Freund, 1991; Matelli and Luppino,
1997). Furthermore, since the electrical excitability of an
area reflects (if reasonable stimulation parameters are used)
the presence of corticospinal projections, the excitability of
area 6aa indicates that the cortico-spinal fibers originate, in
humans, both from area 4 and from the caudal sector of area
6 (6aa). This pattern of origin of the pyramidal tract is
similar to that in the monkey, where the corticospinal tract
originates from F1 (area 4) and the areas located in the
caudal part of area 6 (F2, F3, F4 and a part of F5) (He et
al., 1993, 1995; Luppino et al., 1994). (c) In both humans
and monkeys the frontal eye field and the digits field of area
6aa are adjacent (see Paus, 1996). This proximity could be
used as a marker for drawing homologies between monkey
and human cortical areas.
An attempt to draw a homology between human and
monkey motor cortex is shown in Fig. 3B. The homology
(compare the areas drawn in the same color in Figs. 1 and 3)
is based, in addition to the points listed in the previous
paragraph, on motor cortex ontogeny and the assumption
that the functional areas delimited by the most ancient sulci
maintain their basic location in the phylogenesis.
The precentral sulcus develops in humans from two separate primordia. During prenatal development, both of them
have a horizontal branch that represents the primordia of
superior frontal sulcus and inferior frontal sulcus, respectively (Turner, 1948). (Note that, typically, in the adult brain
also the precentral sulcus is formed by two separate segments; see Ono et al., 1990.) Considering this dual origin of
the precentral sulcus, we suggest that the superior frontal
sulcus, plus the superior precentral sulcus, represents the
human homologue of the monkey superior arcuate sulcus.
Accordingly, the two areas which occupy the dorsal part of
the precentral gyrus and the caudal part of the superior
frontal gyrus (dorsal 6aa and 6ab) in humans correspond
to monkey areas F2 and F7 respectively. This homology is
supported by cytoarchitectonic data (Zilles et al., 1995).
Similarly, we propose that the inferior frontal sulcus, plus
the ascending branch of the inferior precentral sulcus, correspond to the monkey inferior arcuate sulcus, while the
descending branch of the inferior precentral sulcus (which
in humans abuts the inferior frontal sulcus) corresponds to
the inferior precentral dimple of the monkey. According to
this view, the two ventral motor sectors of human motor
cortex (ventral 6aa and area 44) should be the homologues
of areas F4 and F5, respectively (see, for a similar view,
Petrides and Pandya, 1994). In both species these two areas
are separated by the inferior precentral sulcus (descending
branch of the inferior precentral sulcus in humans, inferior
precentral dimple in monkeys). The monkey homologue of
human area 45 is difficult to assess, because the area defined
in monkey as cytoarchitectonic area 45 is an area related to
eye movements (Suzuki and Azuma, 1983; Bruce et al.,
1985). On the other hand, the interesting possibility of a
development of area 45 from 44 (and, therefore, from monkey F5) is challenged by the presence in area 45 of a clear
granular layer.
The most difficult sector of human agranular frontal cortex to which to attribute a homology with the monkey cortex, is represented by the agranular cortex caudal to the
middle frontal gyrus. This sector is often considered to be
the homologue of the monkey ‘dorsal premotor cortex’ on
the basis of the assumption that the monkey superior precentral dimple somehow corresponds to human superior
frontal sulcus. This view, however, is difficult to accept
because of the caudal position of the monkey superior fron-
G. Rizzolatti et al. / Electroencephalography and clinical Neurophysiology 106 (1998) 283–296
293
Fig. 3. (A) Lateral view of human frontal lobe showing the cytoarchitectonic parcellation of Brodmann area 6 according to the Vogts (Vogt and Vogt, 1919)
and the motor representations as determined by electrical surface stimulation by Foerster (1936). (B) Lateral view of human frontal lobe showing a
parcellation of the motor cortex according to the proposed homologies with the monkey motor cortex (see Fig. 1). The homology is based on cytoarchitectonics, electrical stimulation, and sulci embryology. Identical colors in Figs. 1 and 3 indicate areas considered to be homologous. The superior frontal
sulcus (SF) and the superior precentral sulcus (SP) of human brain are drawn in blue as the superior limb of the monkey arcuate sulcus (AS). The inferior
frontal sulcus (IF) and the ascending branch of the inferior precentral sulcus (IPa) of human brain are drawn in red as the inferior limb of the monkey arcuate
sulcus (AI). The descending branch of the inferior precentral sulcus (IPd) is drawn in green as the inferior precentral dimple of the monkey brain. IFG,
inferior frontal gyrus; MFG, middle frontal gyrus; SFG, superior frontal gyrus.
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G. Rizzolatti et al. / Electroencephalography and clinical Neurophysiology 106 (1998) 283–296
tal dimple which starts at the border between F1 (area 4) and
F2 (area 6), and especially because in the monkey this dimple represents the border between the leg and arm fields.
This is certainly not what the superior frontal sulcus delimits
in humans.
Given these facts, our suggestion is that the middle region
of human agranular frontal cortex is the homologue of the
arm field of monkey F4 as well as, inside the ascending
branch of the inferior precentral sulcus, of F5ab. This attribution is supported by the proximity of the representation of
digit and eye movements in both species. Furthermore,
according to this proposal, the development of speech determined in humans an enormous expansion of the mouth
fields of areas homologous to F4 and F5. This expansion
is reflected in part by the increase of the lowest part of
human area 6 (for speech executive aspects) and even
more by areas 44 plus 45 (for its more cognitive functions).
The human homologues of the monkey cortex corresponding to the arm field of F4 and the hand field of F5 (mediating
object to hand action transformation) maintained its middle
location caudal to the location of the field for eye movement.
All interspecies homologies, especially when the human
brain is involved, are very tentative. However, the general
similarity of the organization of the motor cortex of human
and monkey, as outlined above, is encouraging. It should
represent a strong stimulus for further research in the morphology of the human cortex, especially considering the
present availability of a large number of new histochemical
and neurochemical techniques, and for devising new appropriate tests in brain-imaging experiments.
Acknowledgements
Supported by EC Contract n-BMH4-CT95–0789 and
MURST.
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