Mental motor imagery: a window into the representational stages of action

Marc Jeannerod and Jean Decety

INSERM Unit6 94, Bron,

The physiological basis of mental states can be effectively studied by combining cognitive psychology with human . Recent research has employed mental motor imagery in normal and brain-damaged subjects to decipher the content and the structure of covert processes preceding the execution of action. The mapping of brain activity during motor imagery discloses a pattern of activation similar to that of an executed action.

Current Opinion in Neurobiology 1995, 5:727-732

Introduction: motor representations increases with respect to rest. When this is the case, elec- trornyographic (EMG) activity is limited to those muscles Most of our actions are driven indirectly by internally that participate in the simulated action, and tends to be reprsesented goals, rather than directly by the external proportional to the amount of imagined effort [lo]. The environment. Until recently, the existence and structure fact that muscular activity is only partially blocked during of such motor representations were inferred from the simulation of movement suggests that motoneurons are duration and timing of a reaction, or from the pattern of close to threshold. executed movements [l]. Now, however, a more direct approach has been adopted that exploits the unique In several other motor imagery experiments, however, ability of human subjects to image and simulate actions EMG is quiescent (e.g. [ll]). This does not necessarily consciously [P-4]. Motor imag,ery is a cognitive state that contradict the link between motor imagery and muscular can be experienced by virtually everyone with minimal activity, as it may merely reflect better inhibition of training. It corresponds to many situations experienced movement execution under certain conditions or in in everyday life, such as watching somebody’s action certain subjects. with the desire to imitate it, anticipating the effects of an action, preparing or intending, to move, retiaining from This reasoning was confirmed by a recent study of moving, or remembering an action [5*,6]. spinal excitability during motor imagery. Bonnet f’1 al. (M Bonnet, J Decet); J Requin, M Jeannerod, Using motor iniagefy as a means of analysing covert unpublished data) instructed subjects either to press processes seems justlhed by previous work on mental isometrically on a pedal or to simulate mentally the imagery in other modalities. Visual imagery engages same action, with two levels of force (weak and many of the mechanisms and neural structures employed strong). Monosynaptic reflexes were increased during in visual perception [7,8,9’]. It seems logical, therefore, mental simulation in the leg involved in the simulated to look at the motor system for the same direct continu- movement, and this increase was more marked for ity between mechanisms for the representational stages a strong simulated pressure than for a weak one. of action and (action) performance. The experimental The increase, which was more marked for tendinous arguments reviewed below will demonstrate that a (T)-reflexes than Hoffnlann (H)-reflexes, was only motor image is endowed with the same properties as slightly less than the reflex Llcilitation associated with the those of the corresponding (normally covert) motor current performance of the same movement. Whereas reprt-sentation. Namely, it has the same functional both reflexes are conveyed through the same pathways, relationship to the represented action, the same causal the effect of the stimulus is significantly different: the role in the generation of that action, and shares COI~IIIOII H-reflex, which is triggered by the electrical stimulation mechanimls with motor execution. of Ia fibers, by-passes neuromuscular spindles, whereas the T-reflex is a response to stretching those spindles. A Physiological correlates of motor imagery selective increase in excitability of the T-reflex during motor imagery, possibly due to an increase in gamma MerItal simulation of n1ovement activates motor path- nlotoneuron activity, emphasizes the role of spindle Way:;. During motor imagery, muscular activity ofien afferents, not only during movenlent execution, but also

Abbreviations EEC--electroencephalography; EMC-electromyography; fMRI-functional magnetic resonance imaging: H-reflex-Hoffmann reflex; Pco2-CO2 pressure: PET--positron emission tomography; SMA--supplementary motor area; T-reflex-tendinous reflex.

0 Current Biology Ltd ISSN 0959-4388 727 728 Neural control

for organizing the motor output during self-generated actions (121. (a) Respiration Activation of descending motor pathways during mental simulation of movement or related processes is also sug- gested by experiments measuring cortical responsiveness to transcranial magnetic stiuiulation. Pascual-Lcoue ct (II. [lP] found that the size of the area responding to finger movenlents increases as simulated movements are repeated over training periods, in the same way as when o,,,,,,,,,,,, actual movements are repeated. In addition, Gandevia Rl R2 R3 R4 El E2 E3 E4 ES Eb E7 RV and Rothwell [14] have shown that ‘conceutrating’ ou (b) oue hand muscle without activating it increases the ef&ct End tidal PC,,, of subthreshold magnetic stimulation of the cortical area CmmHg) corresponding to that specific muscle. Thus, there is a selective enhancement of responsiveness to stimulation of motor cortical areas during motor imagery. A recent experiment supports this notion tin-ther. Subjects were requested to observe grasping nlovements performed by au experimenter. During the observation period, a transcranial magnetic stiululus was applied to their motor cortex. The pattern of muscular response to RI R2 RJ R4 El E2 E.i E4 E5 Eh E7 RV this stimulus was found to be selectively iucreascd. 111 addition, Fadiga rt (I/. [l?P] observed that the set of --&- Actual -&--Mental muscles activated by the stimulus was the same as that used by the subjects when they actually performed the Fig. 1. Ventilatory effects of mental motor imagery. In this cxpcr- movement. This suggests a conmon neural basis ti,r iment, subjects (n = 10) were requested to produce a phy\iral cf. imitation, observational learning and motor imagery (see fort (pedalling with the right foot against a 15 kg load) ior .! mn, below). and then mentally simulate the same exercise ior the same dw ration. Instructions were to Stan pedalling at a rate oi -1 Hz md then to increase the frequency up to suhmaxlmal eifort. The noi\c These results raise the problem of the mechanism and of the ergometer while the subject performed the nctua c#ort WA\ the locus of motor inhibition during motor imagery. tape-recorded and played hack to the subject during the mental WS- During motor preparation, the movenleut ic blocked sion. (a) Respiration rate and (b) end-tidal f’CCIL were sampled c’vcry by a massive inhibition acting at the spinal Ievcl to 17.5 s. Rl -R4, rest; El -E7, efiort; RV, recovery. Note the sharp IW crease in ventilation at the onset of effort, and the graded in< rc’asc protect motoneurons against a premature triggeriug of during cxerc isc, both actual and mental. Also note the drop in I’( Cl> action-hence the decrease of spinal reflexes during the during mental effort as a result of increased ventilation in the 31). preparatory period and their re-increase shortly before bencc of metabolic demands. Adapted from [I 81. the movement starts [ 1h] During mental sinlulation, it is likely that the excitatory motor output generated is thus part of motor prograiiiniitig. It ir tiiiicd to begill for executing the action is counterbalanced by another, whcii motor activity starts. which represents dtl optiui,J parallel, inhibitory output. The competition between mcchanisnl for anticipating the iorthcoming nletabolic two opposite outputs would account for the partial changes and shortening the intrinsic delay nccdcd f&r block of the nlotoneurons, as shown by residual EMG heart and respiration to adapt to effort (review:cd ill [? 11). recordings and increased reflex excitability. It is uot yet possible to identi6 whether this iuhibitory output The possibility that these autouomic chauges arc‘ .I originates in the cortex or elsewhere. consequence ofmuscular activity can be ruled out bv the spectroscopic analysis performed by rkcty ct (I/.1 I 81. The autonomic system, normally not submitted to vo- which shows uo change in muscular metabolisnl during untary control, is also activated during motor imagery. mental sinlulation. In fact, the combination of illcrt,ascd Heart rate, respiration rate and end-tidal I’,-+ (COG respiration rate and unchanged muscular ~nctabolisln pressure) were measured in subjects actually performing duriug mental siuiulatioii results in a progrcs\ivc droll or mentally simulating a leg exercise 117,181. After only of I~(:~~2 in this condition (Fig. 1): thih uc’vc’r hnppcl~\ a few seconds of actual or mental exercise, heart rate during physical efiort, where veutilatiorl elinlmates (:O> began to increase up to about .50% and 32% over the at about the same rate as it is produced, .111d \\herc resting value, respectively. Respiration rate also increased Pc:o2 remains constant. Recent work by <;mdevin cf almost without delay during actual etli,rt and during (II. 1231 also supports this explanatiou: they observed mental simulatiou [1’9*1_ These results confirm that a graded cardiovascular changes iii curnrized subjects large fraction of the fast increase in heart aud respiration attempting muscular contractions, a situation close to rates at the onset of exercise (both real and mental) motor inlagery. As paralysis was coulplctc, the chnrlgc~ is due to central fictors rather thau metabolic changes could not be due to residual muscular activity and h.rd [20]. Vegetative activation during preparation ti)r etl&-t to be of a ceiitral origin. Jeannerod and Decety - Mental motor imagery 729

Br,ain activity mapping during motor imagery - Motor imagery in the left hemisphere

Pioneering studies using two--dinlensional regional cere- Ml bra.1 blood How (2-D rCHF) mapping or single pho- ton emission computed tomography (SPECT) have emphnsizcd the activity of several brain areas during motor imagery [23-X3]. Prefioritnl areas. supplementary motor arca (SMA), cerebellum nnd basal ganglin are the main activated nrcns. Recent positron emission tomography (PET) studies reveal that brain activity is in t&t intlucnced by the nature ofthe imqinal tnsk. Dcccty c’t (II. 1271 instructed subjects to imagine themwlves grxping visunlly presented three-dilllellsionnl objects wilth their right hand. This mongly activated Brodman~l xxx 6 111the inferior pxt of the frontal LTrus on both sides x well as area 40 in the corltmlnteral inferior VAC VPC pnrict:ll lobule. Subcorticall~, the cnudate I~LIC~CUS\vas k)und to be activated on both sides nnd the ccrebcllum on the left side. Another fi>cu< ofactivity \vas obscrvcd in leti: prefrontal arms. estmding to the dorrolnternl frontnl cortex (areas 9 md 40). Finnlly. the anterior cingulate cortcs (areas 24 md 32) wnc bilaterally nctivntcd.

In othrr studies, where the rask consisted of repetitive, internally generated eye 1281 or hand [ ?P] ii~ovcmc’iits, AC ~11 additionnl nctivntion of SMA was observed. Intcrest- mgly. comparison of esternnlly and internally genernted movements in the smle subjects showed that SMA nctivntiw during simulnted movmwnt~ wns more rostra1 th:ln con~monly observed during otccuted movemmts [20**,3 I]. This finding rciniorces the notion that SMA is divided into nrcns of di#erent hicmrchicnl stntu\ with different fimctionnl implications: the posterior zone is p~~rcly cxcutivc (the SMA proper) 131 ], whcrc,ls the Fig. 2. Patternof cortical activation during mental motor imagery in normal whlccts. The maln Rrodmann areas ac-tivated during mo- more mtcrior zone is lnorc related to rcprcsentntionnl tor imagery have heen outlined on srhcmatlt vwws of a left heml- stqes of .iction niid to Inotw iiiingery [29**]. sphere. Note the consistent Involvement of pre-motor area 6, with- out involvcwent of primary motor cortex (Ml ). The AC-PC (anterior Consciously reprtwntiiig dii action thus involves d comn~lssurc to postcxrior comn~lssurc) line dcf~nes the horizontal ref- pattern of brain activatioli that rcwmlbles that of ercnc c plant in the magnetic rcsonanr cx inlaging (MKI) scan. The nn intcntioixilly executed ,iction (Fig. 2; see’ e.g. vertical tine pawng through rhe AC (VAC) dcflnes a vetiicofrontal plane. WC I\ the vertical line passing through the PC. Data taken [31!*]). Whcthcr primary motor cortex is 3150 ,ictivnted from [27,29**,34*]. during iilingtq still rcmniils uiicertniii. Ckorgopoulos c’t ‘11. 1.131 fo~md thx the activity ot‘ cortical cells in :I wlcctivc c’nhmct’ment of neural nctivitv in those ilionlw~ primar): motor cortex was modified during the nlotor path\vavs conccrncd mith the Gnulated action. prcpamtor): pcmod of J reaching movenlt‘nt dircctcd This Icnds to ,I, increae in ~nusclc strength [ 1 l] and n tomxd n memorized t.irgct III humans, hommw. in dccrcnsc in the vnrinbilit); of movclmIlts [.X3”]. These spite ot‘ thr clcnr nctivation of dtwcnding cortico5piinl rcwlt5 hnvc ilnportnllt implicntiom tbr the nlechnnisms pnth\\-nvs described above, iliost resenrchcrs fi)~lnd no of 1notor lenming. As wlcctivc ilnprovtwltmts in motor activity in cnudnl area 1 during iningined movcnleilts pcrtimmnce cm be obtSCwd in the ,Ibsmce of nn when ~islng PET [37.2’)**,34*] or fkictioilal ningnc%c incre,i\e ill lmscular activity (and thcr&rc without

rcson;1ncc imaging (tMl11) [ 3.5,30]. (For ~111csccption, rc-ntkrcmt input front the ~LISC~C~), they suggest that

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closely similar [2] provides a means for verifying this control for this, Dominey et al. [39**] compared patients’ prediction. Accordingly, a pathological condition that performance during two mental rotation tasks: letter slows movements, for example, should also increase rotation, where the time to decide whether the letter mental movement time for simulating the same move- was normal or mirror-oriented was measured; and hand ments. rotation, where the response depended on whether the hand shown was right or leti. Chronometric studies Mental movement times were compared in normal suggest that the latter task is resolved by the subjects subjects and Parkinsonian patients by Dominey ef a/. mentally making an implicit movement with their [39”]. Patients were selected at the early stage of own hand until it matches the presented hand [40]_ their disease, when they had a predominantly akinetic Parkinson patients were slower for hand rotations than syndrome and presented essentially unilateral signs (on for letter rotations, and their performance in hand the right side). Normal subjects and patients were rotation correlated with their poor imagery performance instructed to perform, with either hand, a sequential in the sequential finger movement task. finger movement (touching the pad of the thumb with the pad of the other four fingers) in conditions of motor Hemiplegic patients are also mentally slower with their execution and motor imagery. Parkinsonian patients impaired arm [41]. Recently, a patient with progressive were slower than normals in all conditions; during motor hemiparesis in the left arm due to a right rolandic execution, their movements were slower than normals lesion was tested for her ability to reproduce, both in both hands, although this effect was more marked in physically and mentally, finger, wrist, elbow and shoulder the right (primarily affected) hand. The same slowness movements displayed by the experimenter. The left arm and asymmetry was observed for mental movements. was slower in executing motor tasks with the fingers and The degrees of asymmetry in both motor execution elbow, but not with the shoulder. The same difference, and mental imagery were significantly correlated (Fig. 3). with the same effecters, was observed for mentally This result stresses the problem that Parkinsonian patients simulated movements [42]. It thus appears that although have in controlling their internal states and, particularly, a motor cortical lesion does not affect the ability to in using internal cues for shifting between states, as this generate motor imagery, it impairs mentally performed is required for execution of a sequential task. actions to the same extent as real movements.

Parkinson &dents A perspective on apraxia Asymmetry 0.075 index 0.050 0.025 Apraxic patients become impaired when they have to 0 imitate actions, reproduce actions from memory or 4.025 pantomime symbolic gestures (the so-called ideomotor -0.050 apraxia) [43,44]. They also have difficulties in rec- -0.075 ognizing gestures and discriminating between gestures -0.100 performed by another person [45]. A patient (LL) with a 4.125 bilateral posterior parietal lesion described by Sirigu cl al. -0.150 [46*] illustrates these points. Hand and finger movements were inadequate when LL was instructed to use an -0.200-O object out of context, such as to perform the gesture Non-visual Non-visual of eating soup with a spoon. The spoon was grabbed incorrectly and was turned several times in the fingers.

Fig. 3. Histogram demonstrating the slower of motor execution and LL’s problem was not a pure hand-shaping deficit, as motor imagery in Parkinson disease patients. Movement time was finger posture was correct when she took the object, measured in right-sided hemi-Parkinson patients (n = 7) and right- not for demonstrating its use, but for handing it over to handed normal controls (n = 71, during a sequential motor task the examiner. The deficit also extended to recognition (touching the tip of the thumb with the tip of the other fingers, five times in a row) in three different conditions: actual performance un- of correctness or incorrectness of hand postures during der visual control (Visual) and without visual control (Non-visual), object use by the examiner. Finally, LL was equally poor and mental performance (Imagined). Measurements were taken be- at verbally describing hand postures in relation to unseen tween a verbal ‘go’ signal preceded by a ‘ready’ signal, given by the objects. experimenter, and a verbal ‘stop’ signal given by the subject. Both hands were tested, and an ‘asymmetry index’ was calculated, with These findings support the notion that the motor positive values indicating faster performance with the right hand, and negative values indicating faster performance with the left impairments observed in apraxic patients result from hand. Note a rightward (non-significant) bias in control subjects. a specific alteration in their ability to mentally evoke Parkinson patients, by contrast, showed a much faster performance actions, or to use stored motor representations for with the left (unimpaired) hand. The same variation was observed forming mental images of actions. Thus, the deficit under all three conditions. Adapted from [39*‘]. arises when the patient shifts from a strategy where object-oriented actions are processed automatically, to Impaired motor imagery in patients with Parkinson when the content of these actions has to be explicitly disease could, however, have resulted from a general represented. A further logical step would be to examine difficulty in generating mental images. In order to apraxic patients for their ability to generate motor Mental motor imagery Jeannerod and Decety 731 imagery, with the idea that their deficit in selecting and mental imagery activates topographically organized visual organizing motor ‘memory’ will also be revealed when cortex. PET investigations. / Cogn Neurosci 1993, 5:263-287. evoking actions mentally [47]. 9. Roland PE, Culyas B: Visual imagery and visual representation. . Trends Neurosci 1994, 17:281-287. The same could be true for a related disorder, con- This paper presents evidence for a cortical network for visual imagery, structional apraxia, also frequently observed following involving parieto-occipital and temporo-occipital association areas, hut not the primary visual cortex. The discrepancy between these results and parietal lesions. Patients have no problem recognizing, those of other authors (e.g. [El), who have iound involvement of primary identieing or naming objects. Yet, they cannot re- visual cortex, is the subject of an interesting debate in the same issue of produce the same objects by drawing, especially when Trends in Neuroscience. requested to perform three dimensional drawings for 10. Wehner T, Vogt S, Sradler M: Task-specific EMC characteristics complex objects or geometrical figures. Patients seem during mental training. Psycho/ Res 1984, 46:389-401. to have lost the ability to process visual information 11. Yue C, Cole KJ: Strength increases from the motor program. for interacting with objects [48*], or to identify correctly Comparison of training with maximal voluntary and imagined muscle contractions. / Neurophysiol 1992, 67:lll &1123. the object attributes needed for object-oriented actions [3]. Accordingly, it can be predicted that these patients 12. Porter R, Lemon R: Corticospinal Function and Voluntary Movement. Oxford: Clarendon Press; 1993. shou1.d have no problem in evoking visual images of objects, whereas they should be unable to simulate 13. Pascual-Leone A, Dang N, Cohen LC, Brasil-Neto J, . . object-oriented actions mentally. Cammarota A, Hallett M: Modulation of motor responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. I Neurophysiol 1995, 74:1037-1045. Conclusions Subjects phystcally or mentally practiced a five finger piano exercise for 2 hours a day ior 5 days. Mental practice alone led to significant improvement in performance. Transcranial magnetic stimulation revealed We have shown converging evidence for a similarity rhe same plastic changes in the motor system as those occurring with the of neural processes involved in central representation acquisition of the skill by repeated physical practice. of actions and motor imagery. This points to motor 14. Candevia SC, Rothwell 1: Knowledge of motor commands imagery as a direct means of accessing the mechanisms and the recruitment of human motoneurons. Brain 1987, of a&on preparation and imitation. 110:1117-1130.

15. Fadiga L, Fogassi L, Pavesi C, Rlzrolatti G: Motor facilitation . . during action observation. A magnetic stimulation study. Acknowledgements / Neurophysiol 1995, 73:2608-2611. This study was based on experiments in monkeys, showing that This work was supported by UnivrrcitO Claude Bernard (Lyon), neurons in ventral area 6 are activated while the monkey watches an experimenter (or another monkey) performing a restricted range of INSEI

24. Roland PE, Skinhoj E, Lassen NA, Larsen B: Different cortical 38. Vogt S: On the relations between perceiving, imagining. and areas in man in organization of voluntary movements in . . performing in the learning of cyclical movement sequences. extrapersonal space. / Neurophysiol 1980, 43:137-l 50. Er / Psycho/ 1995, 86:191-216. This study compares subjects’ performance in rcpllrating complc~x 25. Decety J, Sjoholm H, Rydlng E, Stenberg C, lngvar I>: The movements under diiferent training conditions: physically perioml~ng cerebellum participates in cognitive activity: tomographic the action, visually observing it or mentallv practicing II. Movcmcnl measurements of regional cerebral blood flow. BraN) Res 1990, iorm, spatial scaling and consistency ot rela$ve liming were mca\ured 535:313-317. Ohscrvational and mental training were both eiiec-tivc 111 improvIng

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