The organization of the cortical motor system: new concepts · 3. The general organization of the posterior parietal cortex Anatomically, the posterior parietal cortex is formed by

Invited review

The organization of the cortical motor system: new concepts

G. Rizzolatti*, G. Luppino, M. Matelli

Istituto di Fisiologia Umana, Universita` 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. Inthe 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 movementrepresentation, (b) each motor area plays a specific role in motor control, based on the specificity of its cortical afferents and descendingprojections, (c) in analogy to the motor cortex, the posterior parietal cortex is formed by a multiplicity of areas, each of which is involved inthe 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. Thesecircuits transform sensory information into action. They represent the basic functional units of the motor system. Although these conclu-sions mostly derive from monkey experiments, anatomical and brain-imaging evidence suggest that the organization of human motor cortexis based on the same principles. Possible homologies between the motor cortices of humans and non-human primates are discussed. 1998Elsevier Science Ireland Ltd.

Keywords:Motor cortex; Premotor areas; Parietal lobe; Parieto-frontal connections

1. Introduction

The view on motor cortex organization that dominatedthe second half of this century was rather simple. Roughly,it was the following. In the posterior part of the frontal lobethere are two complete representations of body movements(Penfield and Welch, 1951; Woolsey et al., 1952). The firstis located on the lateral cortical convexity, the other lies onthe mesial cortical surface. The first representation is largeand detailed. It includes the whole of area 4 and most oflateral area 6. This representation is the ‘primary motorcortex’ or M1. The second representation is located on thecortical mesial surface. It is smaller than the former, lessprecise 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 radicallyin the last years. New and more refined anatomical andfunctional techniques have shown, first in non-human pri-

mates and, more recently, (and with much less detail) inhumans, that cortical motor organization is much morecomplex than thought previously. Among the new aspectsof motor organization some are particularly important. Welist them straight away, at the onset of this review, in orderto make it clear its logic.

(1) The motor cortex (defined as the agranular sector ofthe frontal lobe) is formed by a mosaic of anatomically andfunctionally distinct areas. The classical view that there areonly two motor areas is wrong. (2) Like the motor cortex,the posterior parietal lobe is constituted by a multiplicity ofareas with distinct anatomical and functional properties.Each parietal area is involved in the analysis of particularaspects of sensory information. There is no such a thing as amultipurpose area for perception of space or body schema.(3) Motor and parietal areas are reciprocally connected andform 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 theorganization of the cortical motor system and to discuss thepossible functions of the various parieto-frontal circuits.Although most of the reviewed data concern non-human

Electroencephalography and clinical Neurophysiology 106 (1998) 283–296

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* Corresponding author. Tel.: +39 521 290380; fax: +39 521 291304;e-mail: [email protected]

primates, the available data on human cortical organizationconfirm the general validity of the picture presented here.

2. The motor areas of the frontal lobe

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 histo-chemical data (Matelli et al., 1985, 1991). F1 basically cor-responds to area 4 of Brodmann (1909), the other areas aresubdivsions of Brodmann’s area 6. F2 and F7, which lie inthe superior part of area 6, are often referred to collectivelyas ‘dorsal premotor cortex’, while F4 and F5, which lie inthe inferior area 6, are often referred to as ‘ventral premotorcortex’. F3 and F6 form the mesial area 6. (For a review ofthe 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 recordingsand intracortical microstimulation (see below) have demon-strated that the motor cortex contains many functionalmotor representations (motor fields). These motor represen-tations are located in different anatomical areas and not intwo, as classically believed. Their location is shown in Fig.1. The motor representation of F7 is not fully established. Itis known, however, that its dorsal part is devoted to thecontrol of eye movements (supplementary eye field, SEF,Schlag and Schlag-Rey, 1987).

The multiplicity of motor fields presented in Fig. 1 is ingood accord with recent studies of corticospinal projections(He et al., 1993, 1995). Following injections of retrogradeneural tracers into the cervical segments, marked neuronswere found in the arm fields of F1, F2, F3, F4 and F5. Wheninjections were made into the lumbar segments of the spinalcord, labeling was found in the leg fields of F1, F2 and F3.Among the frontal motor areas, two – F6 and F7 – arevirtually devoid of corticospinal neurons. Their main des-cending projections terminate in the brain stem (Keizer andKuypers, 1989).

The connections among the various motor areas show apattern consistent with the organization of corticospinal pro-jections. The two areas that do not send corticospinal pro-jections (F6 and F7) do not send projections to F1 either,being connected only with the motor areas located rostral toF1 (F2, F3, F4 and F5) (Barbas and Pandya, 1987; Luppinoet al., 1993). Conversely, F6 and F7 receive a strong inputfrom the prefrontal cortex, a finding suggesting that theyrepresent the main entrance of the prefrontal input to themotor cortex (Barbas and Pandya, 1987; Luppino et al.,1993; Lu et al., 1994). All motor areas rostral to F1 arelinked one with another. Their connections, however, arenot random, but selectively link fields with similar functions(Dum and Strick, 1991b; Luppino et al., 1993). Finally, theeye movement representation in F7 is strongly connected tothe frontal eye fields (Huerta and Kaas, 1990; Luppino et al.,

1990). In contrast, it has no connections with other motor(skeletomotor) fields.

3. The general organization of the posterior parietalcortex

Anatomically, the posterior parietal cortex is formed bytwo lobules: the superior parietal lobule (SPL) and the infer-ior parietal lobule (IPL). The areas forming the posteriorparietal cortex are shown in Fig. 1.

An important finding that emerges from recent anatomi-cal and functional experiments is that in the posterior par-ietal lobe, as in the motor cortex, there is multiplicity ofarm, leg and face representations. In particular, the arm(the skeletomotor representation best studied) is representedat least 8 times (see Fig. 1).

For a long time it was believed that IPL is related to bothvisual and somatosensory information, while SPL is exclu-sively related to the somatosensory one. Recent data haveshown that this picture is incorrect. There is now evidencethat both lobules receive somatosensory and visual inputs.The modern view is that the posterior areas of both SPL andIPL process predominantly visual information, whereas theanterior areas are related to somatosensory modality in SPLand to an integration of somatosensory and visual informa-tion 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 elementsof the cortical motor system. The general pattern of thesecircuits is the following. Each motor area receives afferentsfrom a specific set of parietal areas. The input from one areais rich (‘predominant’ input), while that from the other areasis moderate or weak (‘additional’ inputs). In turn, each par-ietal area is connected with several motor areas, but hasprivileged contacts with one only. Exceptions to this arearea PFG, which sends an approximately equal amount offibers to several motor areas, and V6A which projects to twoof them. Parietal and frontal areas linked by a ‘predominant’connection have similar functional properties, whereas thissimilarity is not so obvious if one compares the functionalproperties of areas linked by ‘additional’ connections.

If one takes into account the ‘predominant’ connectionsbetween parietal and motor areas, a series of segregatedparieto-frontal functional circuits can be distinguished.Each circuit is involved in a specific sensory-motor trans-formation for action and, thus, represents the functional unitof the cortical motor system (see Rizzolatti et al., 1997b).

Table 1 lists the ‘predominant’ and ‘additional’ afferentsfrom SPL and IPL of each motor area and their other, mostimportant, postrolandic connections. Parieto-prefrontal cir-cuits 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 posteriorparietalcortex. Motor areas are defined according to Matelli et al. (1985, 1991). The terminology used derives from that used by von Economo for the human cortexthat indicates all the frontal areas, including the motor ones, with the letter F. At variance with von Economo, numbers, instead of letters, identifythe variousareas. All parietal areas except those buried within the intraparietal sulcus are defined according to Pandya and Seltzer (1982). The areas located within theintraparietal 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 partof 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 alsodefined according to physiological criteria. The superior arcuate sulcus (AS), the inferior arcuate sulcus (AI) and the inferior precentral dimple are drawn inblue, 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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scope of the present article. Fig. 2 shows the ‘predominant’connections between the posterior parietal areas and themotor areas.

5. PE-F1 circuit

It is a classical notion that area PE (area 5) is a higher-order somatosensory area mostly devoted to the analysis ofproprioceptive information. The most effective stimuli formany PE neurons are specific combinations of multiple jointpositions or combinations of joint and skin stimuli (Sakataet al., 1973; Mountcastle et al., 1975). Recently, Lacquanitiet al. (1995) provided evidence that many neurons in areaPE encode the location of the arm in space in a body-cen-tered coordinate system. The main role of PE-F1 (M1) cir-cuits (Fig. 2A) appears to be that of providing F1 withinformation on the location of body parts necessary forthe control of movement of limbs and other body parts.The notion that PE-F1 is a skeletomotor circuit is supportedby anatomical data showing that, in contrast to the posteriorSPL areas, PE does not receive visual inputs (see Caminiti etal., 1996).

In addition to input from PE, F1 receives connectionsfrom motor areas F2, F3, F4 and F5. F1 is the area thatplays a major role in segmenting actions planned by othermotor areas into elementary movements, and is virtuallyunique among the motor areas in controlling independentfinger movements (see Porter and Lemon, 1993).

6. Inferior area 6 (‘ventral premotor cortex’) circuits

The inferior sector of Brodmann area 6 is constituted bytwo distinct areas: F4 and F5 (Matelli et al., 1985). Recentcytoarchitectonic and immunohistochemical findings haveshown that area F5 is not homogeneous but is formed by twomajor sectors (Matelli et al., 1996). One is located on theposterior bank of the inferior arcuate sulcus (F5 of the arc-

uate bank, F5ab), the other is located on the cortical con-vexity immediately adjacent to the arcuate sulcus (F5 of thecortical convexity, F5c). Functional data confirm this mor-phological subdivision. Each of the 3 subdivisions of infer-ior area 6 is part of a different parieto-frontal circuit. Theproperties of the 3 circuits will be dealt with separately inthe 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 projectionsfrom various areas belonging to the ‘dorsal visual stream’(among them areas MST and MT) that are involved in theanalysis of optic flow and motion (Maunsell and Van Essen,1983; Ungerleider and Desimone, 1986; Boussaoud et al.,1990). In addition, VIP receives somatosensory informationfrom areas PEc and PFG (Seltzer and Pandya, 1986).

VIP neurons fall into two main categories: purely visualneurons and bimodal, visual and tactile, neurons (Colby etal., 1993; Bremmer et al., 1997). Purely visual neurons areoften selective for expanding or contracting visual stimuli.Others are strongly selective for the direction and speed ofstimuli moving along the sagittal plane. Bimodal neuronsrespond independently to visual and tactile stimuli. Theirtactile receptive fields (RFs) are located predominantly onthe face. Their visual RFs are located in parts of the field ofvision corresponding to the tactile RFs (e.g. tactile RF onthe right side of the upper face, visual RF in the right upperquadrant of the visual field). Many neurons respond tovisual stimuli only when they are located in the spacearound the body (peripersonal space). In about one thirdof visually-responsive neurons, the visual RF is encodedin egocentric and not in retinal coordinates (Bremmer etal., 1996). That is, regardless of where the gaze is directed,the visual RF remains in the same location with respect tothe body.

The main target of area VIP in the frontal lobe is area F4(Fig. 2B; Matelli et al., 1994). Microstimulation experi-ments have shown that in F4, arm, neck, face and mouthmovements are represented (Gentilucci et al., 1988). Armand axial movements are located medially in F4, oro-facialmovements more laterally. Single neuron recordings con-firmed the existence of these various representations (God-schalk et al., 1981; Gentilucci et al., 1988). They showedalso that many neurons fire during reaching movementsdirected toward the body or away from it. Others dischargeduring oro-facial movements. Neurons related to distalmovements are virtually absent.

As in area VIP, F4 neurons can be subdivided into twocategories according to their responses to sensory stimuli:bimodal neurons (56%) and unimodal neurons (44%;Fogassi et al., 1996). However, in contrast to VIP, unimodalneurons are typically tactile, purely visual neurons beingvery rare. Unimodal and bimodal neurons have the samesomatosensory characteristics. Their RFs are rather large

Table 1

Parieto-frontal projections in the macaque monkey

Motor areas Posterior parietal areas Other postrolandicareas

Predominantconnections

Additionalconnections

F1 PE SIF2 – dimple region PEc-PEip PFG CGpF2 – ventrorostral MIP V6A-PFG CGpF3 PEci PE-PFG SII-SIF4 VIP PF-PEip SIIF5 – convexity PF AIP SIIF5 – bank AIP PFG SIIF6 PFGF7 PGm V6A-PG CGpF7-SEF LIP


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 fromareas located in the superior parietal lobule. In this view of the brain the inferior parietal lobule and the occipital lobe have been removed, in orderto show theareas located in the medial bank of the intraparietal sulcus and in the anterior bank of the parieto-occipital sulcus, respectively. (B) Parietal projections fromareas 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 theoccipital 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.


and predominantly located on the face, arm and the upperpart of the body. The visual RFs are located in the periper-sonal space, in register with the tactile fields. In most cases,the visually-responsive neurons respond preferentially tostimuli directed toward the tactile RF. In a large majorityof these neurons (70%) the position of the visual RF doesnot change when the gaze moves. Similarly, the visual RFremains anchored to the tactile RF when the body part, onwhich the tactile RF is located, is moved. Taken together,these properties indicate that in F4 the space is encoded inbody-parts-centered coordinates (Graziano et al., 1994;Fogassi et al., 1996). They indicate also that there is nosingle reference point (head, arm or body midline), but,rather, there is a multiplicity of reference points dependingon 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 circuitindicate that this circuit plays a role in encoding the peri-personal space and in transforming object locations intoappropriate movements toward them.

6.2. The AIP-F5ab circuit

Area AIP occupies the rostral part of the lateral bank ofthe intraparietal sulcus (IPs) in front of area LIP (Fig. 2B).Neurons of this area were studied in monkeys trained toreach and grasp objects of different sizes and shapes. Thetesting was carried out both in darkness and in light. Theresults showed that most of them discharge during graspingof specific objects. Their activity is not influenced by objectposition in space, a finding showing that their discharge isindeed related to hand and finger movements and not toproximal arm movements (Taira et al., 1990; Sakata et al.,1995).

AIP neurons were classified into 3 groups: ‘motor-domi-nant’, ‘visual and motor’ and ‘visual-dominant’ neurons.‘Motor-dominant’ neurons do not show any significant dif-ference in activity when tested in darkness or light, ‘visualand motor’ neurons are less active in darkness than in light,‘visual-dominant’ neurons fire vigorously only when thestimulus is visible. Many visually-responsive neuronswere found to discharge also during fixation of the objects,even when fixation was not followed by a subsequent grasp-ing movement. Finally, in most ‘visual and motor’ neurons,the intrinsic characteristic of the object, effective in trigger-ing 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 wheredistal arm movements are also represented (Fig. 2B; Matelliet al., 1994). F5 neurons discharge during specific goal-directed actions performed with the hand, the mouth orboth. According to the action effective in triggering them,F5ab neurons were subdivided into various classes. Amongthem, the most represented are: grasping, holding, tearingand manipulating neurons. Most ‘grasping’ neurons codespecific types of hand prehension, such as for example,

precision grip, whole-hand prehension, finger prehension.The temporal relation of neuron discharge with hand move-ments changes from neuron to neuron. Some neurons fireduring the last part of grasping, others start to fire withfinger aperture and continue during finger closure, othersare activated in advance of the onset of finger movements(Rizzolatti et al., 1988).

Similarly to AIP neurons, many F5ab neurons dischargeto the presentation of 3D objects, even when no immediateor subsequent action upon the object is allowed (Murata etal., 1997). Recent PET data indicate that a similar activationof area 6 occurs also in humans at the presentation of grasp-able objects such as, for example, tools of common usage(Grafton et al., 1997).

Taken together, the AIP-F5ab data suggest that this cir-cuit plays a crucial role in transforming the intrinsic proper-ties of the object into the appropriate hand movements(Jeannerod et al., 1995). The description of object charac-teristics, possibly in terms of their affordances, is carried outin AIP and then is transmitted to F5ab, where different typesof grips are encoded. The matching between object descrip-tion and type of grip allows the selection of the grip effec-tive for a given object (Gallese et al., 1997). A formal modelof 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 visuo-motor transformation for grasping movements was recentlyoffered by studies in which the two areas were separatelyinactivated (Gallese et al., 1994, 1997). The main effectobserved following independent inactivation of AIP andF5ab was a disruption of the preshaping of the hand duringgrasping. The deficit consisted in a mismatch between thefeatures of the object that had to be grasped and the postur-ing of finger movements. When the monkey was successfulin grasping the objects, the grip was achieved only after aseries of corrections that relied on tactile exploration of theobject. These data clearly show that lesion of the AIP-F5abcircuit does not disrupt the ability to perform graspingmovements, but only the capacity to transform the 3D prop-erties of the object into appropriate hand movements.

6.3. The PF-F5c circuit

Neurons located in F5c are indistinguishable from F5abneurons as far as their motor properties are concerned. Likethose neurons, they discharge during specific goal-directedactions. The visual properties, however, of F5ab neurons aremarkedly different from those of F5c. Their main character-istic is that they discharge when the monkey observesanother individual performing an action similar to thatencoded by the neuron. Object presentation is not sufficientto activate them. Because of this correspondence betweenvisual and motor properties, these neurons were called ‘mir-ror neurons’ (Gallese et al., 1996; Rizzolatti et al., 1996a).

The observed actions that most commonly activate themirror neurons are: grasping, placing and manipulating


objects. Most of them respond selectively when the monkeywatches only one type of action (e.g. grasping). Others firein response to two or more actions (e.g. grasping and pla-cing).

Typically, mirror neurons show congruence between theobserved and the executed action. This congruence can bevery strict, that is the effective motor action (e.g. precisiongrip) coincides with the action that, when seen, triggers theneuron (e.g. precision grip). For others the congruence isbroader. For these neurons, the motor requirements to trig-ger them (e. g. precision grip) are usually stricter than thevisual ones (e.g. any type of hand grasping).

Tracer injections in F5c showed that its predominantinputs come from area PF (Fig. 2C). Neurons with mirrorcharacteristics are certainly present in PF, but their proper-ties have not been yet studied in details (our unpublisheddata).

The discovery of mirror neurons is very importantbecause it suggests an important cognitive role for themotor cortex: that of representing actions internally. Thisinternal representation, when evoked by an action made byothers, should be involved in two related functions: actionimitation and action recognition. It is outside the scope ofthe present review to discuss in detail the data and the the-oretical considerations on which this hypothesis is based(Rizzolatti et al., 1996a; Rizzolatti and Arbib, 1998). It isof 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 morerecently MEG data (Hari et al., unpublished data) all indi-cate that the mere observation of an action activates themotor system of the observing individual. This activationincludes, in addition to the region of the left superior tem-poral sulcus (where in the monkey neurons encoding biolo-gical 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 homoge-neous. Recent evidence suggests, however, that, it shouldbe subdivided into two functional sectors: one locatedaround the superior frontal dimple, the other occupying itsventrorostral part (Raos et al., unpublished data). The twoF2 sectors receive (with some overlap) different parietalinputs (Matelli et al., unpublished data). The sector aroundthe dimple is the target of areas PEc and PEip, while theventrorostral receives its predominant input from area MIP(Fig. 2A).

Like F2, F7 also consists of two distinct functional sec-tors: a medial one and a lateral one. The medial sectorcorresponds to the supplementary eye field of Schlag and

Schlag-Rey (1987). This sector receives its main parietalinput from area LIP (Huerta and Kaas, 1990). LIP-F7(SEF) is a circuit involved essentially in the control of eyemovements. The lateral sector receives its main input fromPGm (Fig. 2A; Matelli et al., unpublished data).

7.1. The PEc/PEip-F2 dimple and MIP-F2 ventrorostralcircuits

In several studies, neurons were recorded from the rostralpart of the medial bank of the intraparietal sulcus (basicallyarea PEip). The results have shown that most of themrespond to somatosensory stimuli (Mountcastle et al.,1975; Iwamura and Tanaka, 1996). Many become activein association with arm movements (Kalaska et al., 1990).Typically, the discharge is stronger when the arm is pro-jected in a certain direction. The directional tuning isusually broad.

In a recent experiment, neurons with very intriguingproperties were described in the medial bank of the intra-parietal sulcus, most probably in the posterior part of areaPEip. These neurons had bimodal, tactile and visual RFs(Iriki et al., 1996). The tactile RFs were located on thearm. The visual RFs extended in the space around the tactileRFs. The most interesting finding was that the visual RFswere not fixed in their extension, but expanded when themonkey prepared for a specific motor action. The functionalproperties of these neurons are, in many aspects, similar tothose of F4 neurons, but not to those found in the F2 dimpleregion (see below). Given that PEip sends ‘additional’ pro-jections to F4, it is possible that this set of neurons projectsto F4 rather than to the area target of PEip ‘predominant’output (see Fig. 2A).

As far as we know, there are no specific physiologicalstudies devoted to the functional properties of area PEc.This area is richly connected with area PE (Pandya andSeltzer, 1982). It is likely, therefore, that area PEc, likePE, is involved in the analysis of somatosensory stimulifor movement organization. Electrophysiological studiesof neighboring regions, in which PEc neurons were occa-sionally recorded, confirm this conclusion (Colby andDuhamel, 1991; Galletti et al., 1996).

While PEip and PEc appear to be mostly involved insomatosensory 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 somatosensorystimulation were frequently recorded in MIP (Colby andDuhamel, 1991). Detailed information on the functionalproperties of this area, however, is lacking. More data areavailable on area V6A. This area represents the dorsal partof the region originally described as area PO (Gattass et al.,1985). About half of V6A neurons discharge in response tovisual stimuli. The remainders discharge mostly in associa-tion with eye or arm movements (Galletti et al., 1996, 1997).In contrast to what is observed in most visual areas, in V6A


there is no magnification of the foveal representation (Colbyet al, 1988; Gattass et al., 1997).

All 4 parietal areas described in this section project toarea F2. As mentioned above, however, their connectionpattern is not the same: areas PEip and PEc project mostlyto the dimple region of F2, whereas areas MIP and V6Aproject to the ventrorostral F2 (Fig. 2A).

The dimple region of F2 is somatotopically organized. Legmovements are represented dorsal to the dimple, while armmovements are located ventral to it (Kurata, 1989; Dum andStrick, 1991a; He et al., 1993; Godschalk et al., 1995). Someanatomical evidence suggests that, within the dimple, there isalso a representation of distal arm movements (He et al.,1993). Functional studies of F2 were mostly focused on themotor properties of its neurons. They showed that some F2neurons discharge in association with movement onset, whileothers become active long in advance of it. It is likely thatneurons showing this anticipatory discharge play a role inmotor preparation (see Kurata, 1994; Wise et al., 1997).Some neurons respond to the presentation of visual stimuliinstructing the monkey on the movement that they have sub-sequently to perform. The percentage of these ‘signal-related’neurons is higher in the rostral part of F2 than in its caudal part(dimple region) (Tanne´ et al., 1995; Caminiti et al., 1996;Johnson et al., 1996).

There is little information on the responses of F2 neuronsto sensory stimuli. Preliminary observations from ourlaboratory indicate that there is a differential distributionof sensory properties within F2. While in the dimple regionmost neurons respond to proprioceptive stimuli, in ventro-rostral F2 neurons respond also to tactile and visual stimu-lation (Raos et al., unpublished data). This functional seg-regation of sensory modalities within F2 is consistent withthe parietal input to the two F2 subregions.

In conclusion, the PEip/PEc-F2 dimple circuit appears tobe involved in planning and controlling arm (and leg) move-ments on the basis of somatosensory information. In con-trast, the MIP/V6A-F2 ventrorostral circuit uses somato-sensory and visual information, probably for the same pur-pose. Monitoring and controlling arm position during thetransport phase of the hand toward the target could be one ofthe major functions of this circuit. The optic ataxia symp-toms that typically result as a consequence of damage tosuperior parietal lobule (De Renzi, 1982; Milner and Good-ale, 1995), fit this hypothesis well.

7.2. The PGm-F7 circuit

Area PGm is cytoarchitecturally similar to area PG (Pan-dya and Seltzer, 1982). It is richly connected with this areaand 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 com-plex area is largely unknown. Area PGm is the major sourceof parietal input to lateral F7 (Fig. 2A).

Recording studies have shown that in F7 there are neu-rons that discharge in relation to arm movements, others thatfire before movement onset, and others active in response tovisual stimuli. Visually-responsive neurons are morenumerous 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 Pellegrinoand Wise, 1991).

Vaadia et al. (1986) tested F7 neurons in a behavioralparadigm in which reaching movements were: (a) triggeredby and directed toward the same visual (or acoustical)source, or (b) triggered by a given sensory source, but direc-ted to a spatial position different from that of this source.They found that some F7 neurons fired exclusively in thefirst condition. They proposed that these neurons contributeto spatial localization of external stimuli for reaching move-ments.

A further function of area F7 is that this area, possiblywith the contribution of F2, plays a crucial role in condi-tional stimulus-response association tasks (see Passingham,1993). Evidence in favor of this hypothesis derives fromablation studies carried out by Halsband and Passingham(1982) and Petrides (1982). Halsband and Passingham(1982) ablated the postarcuate cortex along the superiorand inferior branches of the arcuate sulcus in monkeys pre-viously trained to make arbitrary goal-directed movementsin response to colored stimuli. After the lesion, the monkeyswere unable to execute the task any longer, although noobvious motor deficit was present. Similar results wereobtained by Petrides (1982) following ablation of theperiarcuate cortex in monkeys which also had previouslylearned a conditional association motor task. If one com-pares the lesions made by the two groups of researchers,it appears that F7 and the rostralmost part of F2 were theonly regions damaged in all monkeys. Thus, F7, possiblywith a contribution of F2, appears to play an importantrole in conditional movement selection. Lesion studiesin patients suggest a similar role for the dorsal premotorcortex of humans (Petrides, 1985; Halsband and Freund,1990).

8. Mesial area 6 circuits

Mesial area 6 was classically considered to be a singlearea: the supplementary motor area (Penfield and Welch,1951; Woolsey et al., 1952). Recent cytoarchitectural, his-tochemical, and functional data have clearly shown that inthe monkey the mesial surface of area 6 is occupied by twoareas: F3 or SMA proper and F6 or pre-SMA (Luppino etal., 1991; Matelli et al., 1991). F3 receives its main parietalinput from area PEci (Fig. 2A; Luppino et al., 1993). F6 isthe only motor area that cannot be considered part of aspecific parieto-frontal circuit. While it receives a verystrong input from the prefrontal lobe, it has very littleinput from the parietal lobe (Luppino et al., 1993).


8.1. The PEci-F3 circuit

Area PEci was defined by Pandya and Seltzer (1982) as aparietal area localized in the caudal part of the cingulatesulcus (Fig. 1). Anatomical data from the same authorsshowed that area PEci is connected with areas PE, PEcand PGm. There is only one functional study of this area(Murray and Coulter, 1981). This study showed that in PEcithere is a complete somatosensory map of the body. Becauseof this finding and its anatomical location, PEci was namedthe ‘supplementary sensory area’.

PEci is the main source of input to area F3. Additionalinputs to the latter area come from areas 23, SII and, tolesser extent, SI, PE and PFG (Luppino et al., 1993). F3contains a complete somatotopic representation of bodymovements (Mitz and Wise, 1987; Luppino et al., 1991).The leg field is located caudally, the arm field rostrally. Thearm and leg fields form two oblique bands running from aventro-caudal to a dorso-rostral location. The face field,much smaller than the other two, is located at the rostralend of the arm field.

Single-neuron recordings showed that many F3 neurons(in the case of studies preceding the subdivision of SMAin 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 move-ments. Although the relation between the discharge andmovement may vary greatly from one neuron to another,the discharge onset of F3 neurons is typically time-lockedto the movement onset. Some neurons fire exclusively inrelation to specific sequences of movements (Tanji et al.,1996).

The behavior of F3 neurons is, for many aspects, similarto that of F1 (area 4) neurons. There are, however, someorganization properties that distinguish the two areas: (a) inF1 proximal and distal movement are anatomically segre-gated, while they are mixed in F3, (b) intracortical electricalmicrostimulation evokes body part movements around asingle joint in F1, whereas movements involving two ormore articulations are often observed in F3 (Mitz andWise, 1987; Luppino et al., 1991) and (c) although thereis some controversy on this point (see He et al., 1995), mostauthors agree that in F3 proximal movements are muchmore represented than distal movements (Penfield andWelch, 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 cir-cuit controls motor activity in a global way. A more specificinterpretation of the possible functional role of F3 role inmotor control was advanced by Massion and his co-workers(Massion, 1992). Their view, based on patients’ data, is thatF3 plays an important role in the control of posture and, inparticular, in the postural adjustments that precede volun-tary movements.

8.2. Prefrontal lobe/F6 (pre-SMA) circuit

At variance with all other motor areas, the input that F6(pre-SMA) receives from the parietal lobe is very modest. Incontrast, it receives a substantial input from area 46 andfrom the rostral cingulate cortex (area 24c; Luppino et al.,1993; Lu et al., 1994). This peculiar anatomical organiza-tion suggests that F6, unlike the other motor areas, isinvolved in a control of motor processing of the parieto-frontal circuits, rather than in sensorimotor transformationsfor action execution.

A large body of data, coming both from brain-imagingstudies in humans, and neuron-recording data in monkeys, isconsistent with this ‘supramotor’ function of F6. Anatomi-cal and neurochemical data have shown that in humans (asin monkeys) the border between pre-SMA and F3 (SMAproper) corresponds to a frontal plane passing through theanterior commissure (Zilles et al., 1995). Thus, activationsobserved in human brain-imaging studies anterior to thisplane indicate activations of pre-SMA, while activationsposterior to it indicate activity of SMA proper. Using thislocalization criterion and correlating the activation site withthe examined task, it is clear that while SMA proper isactivated by ‘simple’ movements, pre-SMA requires ‘com-plex’ 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 withprecision the functional role of pre-SMA. A possible clueas to what may be the key factor for activating pre-SMAcomes from monkey studies. Recording of F6 neurons in anatural situation showed that, unlike F4 and F5 neurons, F6neurons do not discharge in association with distal and prox-imal arm movements, but control actions globally. Someneurons discharge at visual presentation of graspableobjects independently of their location, but increase theirfiring as the stimulus is moved toward the monkey. Others,on the contrary, are inhibited at the presentation of thegraspable object, but start to discharge as soon as it isbeing brought close to the monkey. There are several facil-itation/inhibition combinations that characterize differentF6 neurons. What appears to be constant, however, is themodulation of the neuron’s discharge according to whetheran object can or cannot be grasped (Rizzolatti et al.,1990).

The interpretation of these findings that we favor, is thatF6 neurons constitute a system that controls the potentialactions encoded in the lateral parieto-frontal circuits. Nor-mally, even when the neurons encoding these potentialactions are activated, movement does not start. Only whenexternal contingencies and motivational factors allow it, thecontrol system represented by F6 (and possibly by the ros-tral motor cingulate area 24c) renders the onset of move-ment possible. The degree of activity in F6 depends, in turn,on the behavioral situation in which the stimulus is (close-


distant, presence of obstacle, physical possibility to act) andon motivation.

This hypothesis is not in contrast with the notion that pre-SMA may plays an important role in sequence organization(Tanji et al., 1996). It put the emphasis, however, not onsequence per se, but on the particular interplay of facilita-tion and inhibition that motor sequences, especially whencomplex, require.

9. Possible homologies between human and monkeymotor cortex

The new view on cortical motor organization that wepresented in the previous sections is in large part based onmonkey data. While it is immediately apparent from braingross anatomy and cytoarchitectonic data that human corti-cal organization is similar (although obviously of muchgreater complexity) to that of the monkey, nevertheless itis not easy to transfer data from monkey circuits to humancircuits, first, because precise homologies between monkeyand human cortical areas are difficult to establish and sec-ond, because even with the most advanced brain-imagingtechnique developed in the last decade, the degree of detailthat one can obtain in human experiments is incomparablylower than that obtainable in primate experiments.

In spite of these limitations, it is of interest to draw acomparison between human and monkey motor cortices inorder to have a starting point for testing functional hypoth-eses derived from monkey experiments in human subjects,and for better understanding, therefore, human motor cortexorganization.

Fig. 3A shows a lateral view of human frontal lobe, inwhich the cytoarchitectonic parcellation of the motor cortex(Vogt and Vogt, 1919) and the motor representations, asdetermined by electrical surface stimulation (Foerster,1936), are presented. There are 3 aspects of this map thatare worth noting. (a) The surface of the precentral gyrusbelongs mostly to area 6aa and not to area 4 (as frequentlybelieved). Area 4 is buried for most of its extent in thecentral sulcus. This location of area 4 is in agreementwith modern data on this issue (Geyer et al., 1996; seealso Preuss et al., 1996). (b) An ordered movement repre-sentation is present in area 6aa (Foerster, 1936). Thisfurther motor representation on the lateral brain surfaceindicates that motor representation is multiple in humansas in monkeys (see Freund, 1991; Matelli and Luppino,1997). Furthermore, since the electrical excitability of anarea reflects (if reasonable stimulation parameters are used)the presence of corticospinal projections, the excitability ofarea 6aa indicates that the cortico-spinal fibers originate, inhumans, both from area 4 and from the caudal sector of area6 (6aa). This pattern of origin of the pyramidal tract issimilar to that in the monkey, where the corticospinal tractoriginates from F1 (area 4) and the areas located in thecaudal part of area 6 (F2, F3, F4 and a part of F5) (He et

al., 1993, 1995; Luppino et al., 1994). (c) In both humansand monkeys the frontal eye field and the digits field of area6aa are adjacent (see Paus, 1996). This proximity could beused as a marker for drawing homologies between monkeyand human cortical areas.

An attempt to draw a homology between human andmonkey 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 previousparagraph, on motor cortex ontogeny and the assumptionthat the functional areas delimited by the most ancient sulcimaintain their basic location in the phylogenesis.

The precentral sulcus develops in humans from two sepa-rate primordia. During prenatal development, both of themhave a horizontal branch that represents the primordia ofsuperior frontal sulcus and inferior frontal sulcus, respec-tively (Turner, 1948). (Note that, typically, in the adult brainalso the precentral sulcus is formed by two separate seg-ments; see Ono et al., 1990.) Considering this dual origin ofthe precentral sulcus, we suggest that the superior frontalsulcus, plus the superior precentral sulcus, represents thehuman homologue of the monkey superior arcuate sulcus.Accordingly, the two areas which occupy the dorsal part ofthe precentral gyrus and the caudal part of the superiorfrontal gyrus (dorsal 6aa and 6ab) in humans correspondto monkey areas F2 and F7 respectively. This homology issupported by cytoarchitectonic data (Zilles et al., 1995).

Similarly, we propose that the inferior frontal sulcus, plusthe ascending branch of the inferior precentral sulcus, cor-respond to the monkey inferior arcuate sulcus, while thedescending branch of the inferior precentral sulcus (whichin humans abuts the inferior frontal sulcus) corresponds tothe inferior precentral dimple of the monkey. According tothis view, the two ventral motor sectors of human motorcortex (ventral 6aa and area 44) should be the homologuesof areas F4 and F5, respectively (see, for a similar view,Petrides and Pandya, 1994). In both species these two areasare separated by the inferior precentral sulcus (descendingbranch of the inferior precentral sulcus in humans, inferiorprecentral dimple in monkeys). The monkey homologue ofhuman area 45 is difficult to assess, because the area definedin monkey as cytoarchitectonic area 45 is an area related toeye movements (Suzuki and Azuma, 1983; Bruce et al.,1985). On the other hand, the interesting possibility of adevelopment of area 45 from 44 (and, therefore, from mon-key F5) is challenged by the presence in area 45 of a cleargranular layer.

The most difficult sector of human agranular frontal cor-tex to which to attribute a homology with the monkey cor-tex, is represented by the agranular cortex caudal to themiddle frontal gyrus. This sector is often considered to bethe homologue of the monkey ‘dorsal premotor cortex’ onthe basis of the assumption that the monkey superior pre-central dimple somehow corresponds to human superiorfrontal sulcus. This view, however, is difficult to acceptbecause of the caudal position of the monkey superior fron-


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 aparcellation of the motor cortex according to the proposed homologies with the monkey motor cortex (see Fig. 1). The homology is based on cytoarch-itectonics, electrical stimulation, and sulci embryology. Identical colors in Figs. 1 and 3 indicate areas considered to be homologous. The superior frontalsulcus (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 inferiorfrontal 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 arcuatesulcus (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.


tal dimple which starts at the border between F1 (area 4) andF2 (area 6), and especially because in the monkey this dim-ple represents the border between the leg and arm fields.This is certainly not what the superior frontal sulcus delimitsin humans.

Given these facts, our suggestion is that the middle regionof human agranular frontal cortex is the homologue of thearm field of monkey F4 as well as, inside the ascendingbranch of the inferior precentral sulcus, of F5ab. This attri-bution is supported by the proximity of the representation ofdigit and eye movements in both species. Furthermore,according to this proposal, the development of speech deter-mined in humans an enormous expansion of the mouthfields of areas homologous to F4 and F5. This expansionis reflected in part by the increase of the lowest part ofhuman area 6 (for speech executive aspects) and evenmore by areas 44 plus 45 (for its more cognitive functions).The human homologues of the monkey cortex correspond-ing to the arm field of F4 and the hand field of F5 (mediatingobject to hand action transformation) maintained its middlelocation caudal to the location of the field for eye move-ment.

All interspecies homologies, especially when the humanbrain is involved, are very tentative. However, the generalsimilarity of the organization of the motor cortex of humanand monkey, as outlined above, is encouraging. It shouldrepresent a strong stimulus for further research in the mor-phology of the human cortex, especially considering thepresent availability of a large number of new histochemicaland neurochemical techniques, and for devising new appro-priate tests in brain-imaging experiments.

Acknowledgements

Supported by EC Contract n-BMH4-CT95–0789 andMURST.

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The organization of the cortical motor system: new concepts · 3. The general organization of the posterior parietal cortex Anatomically, the posterior parietal cortex is formed by