Clinical Neurophysiology 110 (1999) 799±805

Mental representations of movements. Brain potentials associated with imagination of eye movements P. HoÈllinger a, b,*, R. Beisteiner b, W. Lang b, G. Lindinger b, A. Berthoz c b

a Department of Neurology, University of Berne, Murtenstrasse, CH-3010 Berne, Switzerland Department of Neurology, University of Vienna, WaÈhringer GuÈrtel 18-20, A-1090 Vienna, Austria c L.P.P.A. CNRS-ColleÁge de France, 15 rue de l'Ecole de MeÂdicine, 75006 Paris, France

Accepted 22 September 1998

Abstract Objective: Current research in motor imagery is focused on similarities between actual and imagined movements on a central and a peripheral level of the nervous system. The present study measured slow cortical potentials (DC-potentials) during execution and internal simulation of memorized saccadic eye movements. Methods: In 19 healthy righthanded subjects DC-potentials were recorded from 28 electrodes during execution and during imagination of a sequence of memorized eye movements during a visual imagery condition. Results: Both oculomotor conditions showed a similar global level and similar topography of performance related DC-potentials, both strongly differed from the visual imagery condition and were lateralized to the left hemisphere. Conclusion: This study therefore supports the hypothesis that cortical brain structures responsible for execution and imagination of memorized saccadic eye movements are similar. The observed left hemispheric lateralization is in contrast to a previous study using bimanual movements. This discrepancy is discussed in relation to recent observations in apractic patients with parietal lesions. q 1999 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Motor imagery; Brain; potentials; Eye movements

1. Introduction Motor imagery or internal simulation of movements (ISM) has gained increasing attention since the pioneering work of Decety and coworkers (Decety et al., 1988; Decety et al., 1989; Decety et al., 1990; Decety et al., 1991; Decety et al., 1993; Decety et al., 1994; Decety and Michel, 1989; Decety and Boisson, 1990; Decety and Ingvar, 1990; Decety, 1993; Decety, 1996; Decety and Jeannerod, 1996). Several previous experiments investigated neurophysiological processes underlying ISM (Ingvar and Philipson, 1977; Roland et al., 1980; Breitling et al., 1986; Goldenberg et al., 1986; Decety et al., 1988; Decety et al., 1990; Rao et al., 1993; Stephan et al., 1995). A theory was forwarded that similar brain regions, which are concerned with the actual execution of a movement, are also activated during its mental ideation (Decety and * Corresponding author. Tel.: 1 41-31-632-3392; fax: 1 41-31-6329679.

Ingvar, 1990; Decety, 1996). This hypothesis gained further evidence from neuropsychological observations in normal subjects (Decety et al., 1989; Decety et al., 1993; Decety and Michel, 1989; Decety, 1993), as well as in patients with lesions affecting different levels of the motor system (Decety and Boisson, 1990; Dominey et al., 1995; Sirigu et al., 1995; Ochipa et al., 1997). In these experiments, the performance times of actual execution and of mental imagination for the same type of movement were very closely related. However, those studies yielded contradictory results as to differences in the topographical pattern of cerebral activation between mental ideation and actual execution of a movement. This especially pertains to the question of a joint activation of the supplementary motor area (SMA) and the primary motor cortex (M1). Whereas some studies described a lack of activation of M1 during ISM (Ingvar and Philipson, 1977; Roland et al., 1980; Decety et al., 1988; Rao et al., 1993; Stephan et al., 1995), it was recently shown with positron emission tomography (PET)

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(Lang et al., 1994), DC-potentials (Beisteiner et al., 1995), magnetoencephalography (MEG) (Lang et al., 1996; Schnitzler et al., 1997), functional magnetic resonance imaging (fMRI) (Hallett et al., 1994; Leonardo et al., 1995; Porro et al., 1996; Roth et al., 1996; Bodis-Wollner et al., 1997) and transcranial magnetic stimulation (PascalLeone et al., 1995; Abbruzzese et al., 1996; Kasai et al., 1997; Kiers et al., 1997; Rossi et al., 1998) that ISM does imply an activation of M1. In a similar way, the participation of peripheral effector organs of a movement during ISM remains equivocal, since on the one hand, task-related changes in electromyographic (EMG) activity (Jacobson, 1932 ; Hale, 1982; Wehner et al., 1984; Harris and Robinson, 1986) and in spinal excitability (Oishi et al., 1994; Bonnet et al., 1997; Kiers et al., 1997) have been documented. However, on the other hand, no musculospinal activation during ISM was also reported (Yue and Cole, 1992; Decety et al., 1993; Abbruzzese et al., 1996; Kasai et al., 1997). Another issue in imagery research concerns hemispheric specialization for the different steps underlying imagination of visual objects (Farah, 1984, 1989; Farah et al., 1985; Kosslyn, 1988; Goldenberg, 1989) and of movements (Goldenberg et al., 1986; Beisteiner et al., 1995). In a previous study by Beisteiner et al., performance-related slow brain potentials were signi®cantly larger over the left hemisphere compared with corresponding recordings of the right hemisphere (Beisteiner et al., 1995). Moreover, left hemisphere dominance was signi®cantly larger with internal simulation as compared with execution of bimanual ®nger movements, but not with movements of one hand separately. It was speculated that this difference might be due to larger demands of spatial coordination during ISM of bimanual than of unilateral movements. This ®nding of different cortical activation patterns in execution versus internal simulation of bilateral hand movements contrasted with a previous study of saccadic eye movements (Lang et al., 1994), where no difference between movement execution and internal simulation was observed. Given this discrepancy, hand and eye movement tasks were investigated in the same subjects using the DCpotential method, in order to ®nd out whether different activation patterns in execution versus internal simulation are task-speci®c for hand movements. We will report on the variations of slow brain potentials (DC-potentials) during the execution and mental imagination of memorized saccadic eye movements. Sensitivity of the method to detect systematic variations of DC-potential topography with task qualities was repeatedly shown (Lang et al., 1989, 1991, 1992; Uhl et al., 1990; Beisteiner et al., 1995). Thus, combining the results of the present investigation using DC-potentials and our previous study using PET (Lang et al., 1994) should allow for a multimodal approach to ISM. In that way, one cognitive function can be investigated with different modalities, in order to overcome their technical drawbacks (Uhl et al., 1990).

2. Materials and methods 2.1. Subjects Nineteen subjects (5 females and 14 males; ages ranged 21±30 years) performed eye and hand tasks in one experimental session. Data concerning hand tasks have already been published (Beisteiner et al., 1995), but data on eye tasks are reported in the present article. Subjects gave their informed consent and were paid for completing the experiment. 2.2. Conditions Subjects had to observe and to memorize the movements of a point performing 4 jumps on a monitor. Then they received an instruction visible on the screen which informed them of the following condition to be performed. Three conditions had to be accomplished: Condition E-E: move your eyes according to the sequence (command in German: `Auge B'). Subjects were advised to use the 5 red rings on the monitor to de®ne the amplitudes of eye movements. In this way, eyeballs covered a maximal angle of 58, given that a sequence comprising upper and lower extreme point locations had to be performed. Condition E-I: imagine moving your eyes according to the sequence (command in German: `Auge V') while ®xing your gaze at a small red ring in the middle of the computer screen. Condition Rest: imagine the starting picture of 5 points on the monitor at a standstill (command in German: `Bild').

2.3. Materials The materials comprised the presentation on a computer screen of a starting picture and a point, jumping and thus indicating several directions. Five points measuring 0.8 cm in diameter each were presented vertically in the middle of the screen with equal distances between them (2.9 cm). The 5 points of the starting picture (warning stimulus) were simultaneously visible on the monitor for 1 s. Immediately after the disappearance of this ®rst image, a point appeared on the monitor, performing a sequence of 4 jumps. Each point location was visible for 1 s. A sequence always started and ended with the central point. Each of the 5 possible point locations was indicated throughout the whole experiment by a constantly visible small red ring. After a blocking period of 10 s, one of the instructions (see conditions) appeared on the monitor, which instructed subjects what to do with the sequence seen immediately before. The instruction itself was visible for 2 s and was presented in German.

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2.4. Procedure

2.6. Data analysis

Subjects were comfortably seated in an EEG-chair about 1.5 meters in front of a future computer, which produced sequences as well as instructions. Participants started each trial voluntarily by extending both index ®ngers, which broke a light barrier and thus entailed the demonstration of a sequence on the monitor. After that, they once again made a rapid voluntary upward movement with their index ®ngers and received one of the 3 instructions. This second ®nger extension served as a trigger to start the data acquisition period. When the instruction disappeared they had to perform the task twice in immediate succession with about the same speed as the demonstration of the sequence on the monitor (1 jump/s). Thus, a correct performance required approximately 8 s. Between trials, subjects were allowed to pause whenever they wanted. The order of conditions, as well as the sequences of point movements on the monitor, were randomized. Point jumps were equally distributed among the different directions, so that by averaging across trials the minimal artifacts of eye movements on the EEG were reduced. To avoid artifacts, subjects had to ®x their gaze on the central red ring during the whole period of data acquisition (4 s before and 14 s after the trigger movement, which produced the instruction on the monitor). During the attachment of electrodes, the course of the experiment was explained and subjects were able to practice at the same time.

Imagery conditions E-I and Rest had to be accomplished without any eye or ®nger movements during task performance. Only a few eye or ®nger movements occurred, and in these trials saccades to a target position and back to the ®xation point (but not a whole sequence) were detected. Trials containing such eye or ®nger movements were excluded from further data analysis. Each trial included a recording period of 18 s; the ®rst 4 s being located before the trigger. The baseline was calculated from the ®rst second of the data acquisition period. For an interval between the 8th and the 9th second of the recording time performance-related negative DC-potentials (N-P) were calculated. A linear regression was applied during off-line analysis, in order to remove artifacts in the EEG resulting from eye blinks after identifying them in the vertical EOG by means of a Woods ®lter.

2.5. Data acquisition DC-potentials were recorded from the following 28 electrodes: F7, F3, Fz, F4, F8, FC5 (half-way between F7 and C5), FC1 (half-way between Fz and C3), FC2 (half-way between Fz and C2), FC6 (half-way between F8 and C6), T3, C5 (half-way between T3 and C3), C3, C1 (half-way between C3 and Cz), Cz, C2 (half-way between Cz and C4), C4, C6 (half-way between C4 and T4), T4, CP5 (half-way between C5 and T5), CP1 (half-way between C1 and Pz), CP2 (half-way between C2 and Pz), CP6 (half-way between C6 and T6), P3, Pz, P4, T5, T6, Oz. Electrode application on the subject's head was performed with a specialized technique permitting very stable recording conditions over long time periods without skin temperature in¯uencing DCpotentials (Bauer et al., 1989). Two further channels were used for horizontal (lateral orbital rim of the right eye versus lateral orbital rim of the left eye) and vertical (upper orbital rim of the right eye versus lower orbital rim of the right eye) EOG. In addition, horizontal and vertical eye movements were analyzed by use of an infra-red oculography device (Iris-System, Skalar-Medical). Linked ears (electrodes on the processus mastoideus of each side) served as reference. The frequency band of ampli®cation ranged from DC to 100 Hz. The sampling rate was 200 Hz using a 12-bit analog-todigital converter.

2.7. Statistical analysis With a MANOVA, the question was approached whether the 3 conditions have a different global level of N-P and a different distribution of N-P across the scalp (condition by electrode). Statistics on topographical differences of N-P were based on normalized data (McCarthey and Wood, 1985) and degrees of freedom were corrected by the Greenhouse-Geisser epsilon. For the calculation of hemispheric differences, a MANOVA was used with the within-subject factors condition, hemisphere and region (contrasting corresponding electrodes of the left and right hemisphere). Where appropriate, post-hoc analysis was performed using the t test. 3. Results 3.1. Patterns of DC-potentials during internal simulation and actual execution of eye movements Neither a signi®cant difference of the global level (df ˆ 1:18; F ˆ 0:74; P ˆ n:s:) nor of the topography (df ˆ 5:92; F ˆ 0:92; P ˆ n:s:) of amplitudes of performance-related DC-potentials between E-I and E-E was observed. Fig. 1 displays the close similarity of DC-potentials between the two tasks and shows slightly greater amplitudes for E-E in central and mid-line electrodes, a difference which did not turn out to be signi®cant. Oculomotor conditions showed highly signi®cant differences in their global DC-potential levels (df ˆ 1:18; F ˆ 11:3; P , 0:01), as well as for the 28 electrodes separately (df ˆ 4:73; F ˆ 5:4; P , 0:001) when compared with Rest (Fig. 2 for E-I versus Rest). 3.2. Hemispheric asymmetry In both tasks of the present study, the performance-

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Fig. 1. Course of DC-potentials associated with E-E (solid line) and E-I (dashed line) for 19 selected electrodes (average across 19 subjects). The vertical line at the fourth second (arrow) indicates the second fore®nger extension (trigger movement) which informed subjects about the following condition.

related DC-potentials are lateralized towards the left cerebral hemisphere (df ˆ 1:18; F ˆ 12:21; P , 0:01).The extent of lateralization to the left hemisphere differs among the regions (signi®cant interaction Hemisphere by Region: df ˆ 4:67; F ˆ 11:81; P , 0:001) and is largest in fronto-lateral locations (F7/8, F3/4), as displayed in Fig. 3.

4. Discussion

Fig. 2. Course of DC-potentials associated with E-I (solid line) and Rest (dotted line). For further details see legend to Fig. 1.

ing self-paced saccadic eye movements (Petit et al., 1993), ocular ®xation (Petit et al., 1995), memorized saccades (Petit et al., 1996) and oculomotor imagery (Lang et al., 1994). DC-potentials do not offer the possibility to identify activation foci in the cortex as precisely as PET can do, and particularly deeper brain structures such as the cingulate gyrus or the basal ganglia are inaccessible to the electrophysiological method used herein. However, DC-potentials possess better time resolution properties than PET, which necessitates data sampling up to 80 s (Fox et al., 1985; Kanno et al., 1991). Investigating hand modality (Beisteiner et al., 1995)

4.1. Patterns of DC-potentials during internal simulation and actual execution of eye movements The present observation of no statistically signi®cant difference in amplitude and distribution of cortical electric activity during the execution of voluntary eye movements and their internal simulation supports the assumption that both tasks share similar neural structures (Jacobson, 1932; Wehner et al., 1984; Decety, 1993, 1996; Oishi et al., 1994; Pascal-Leone et al., 1995; Porro et al., 1996; Roth et al., 1996; Bodis-Wollner et al., 1997; Schnitzler et al., 1997). This ®nding further agrees strongly with a PET study dealing with a very closely related paradigm, where subjects had to execute or to imagine horizontal self-paced saccades (Lang et al., 1994). Both tasks signi®cantly activated the SMA, the precentral and the median cingulate gyrus; brain areas which therefore seem to constitute a network mediat-

Fig. 3. Lateralizations with E-E and E-I. Displayed are mean differences of DC-potentials between corresponding electrodes of the two hemispheres. *P , 0:05.

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yielded signi®cantly larger negativities during execution of a bimanual hand movement than during its imagination in several central and mid-line electrodes. This observation seems to con®rm previous studies (Roland et al., 1980; Decety et al., 1988; Roth et al., 1996), reporting greater neural activity during motor execution than during ISM. In the present study, DC-potential amplitudes are slightly larger with actual execution of eye movements than with ISM, especially in central leads, which is evident on a descriptive level of data analysis (Fig. 1) but does not turn out to be statistically signi®cant. An apparently slighter difference between execution and imagination of eye movements compared with hand movements might be attributed to the smaller topographical extension of the cortical neuron population subserving eye movements (Fox et al., 1985). This problem therefore, concerns a mixture of amplitude and topography effects in relation to spatial resolution of the detector system, as it was pointed out for PET by Fox et al. (Fox et al., 1985). The notion that motor execution leads to higher levels of neural activity than ISM as expressed by rCBF or DC-potential amplitude is also supported by a study in patients with intractable epileptic seizures who underwent subdural electrode placement on the medial surface of the cerebral hemispheres for evaluation of surgical treatment (Fried et al., 1991). During electrical stimulation mapping, several patients reported an experience of movement in the absence of any overt motor activity. In particular, the patients' feeling of a movement without any observable motor act seems to match the description of a kinaesthetic representation of movement, i.e. the mental ideation of movement in the ®rst-person perspective (Hale, 1982; Harris and Robinson, 1986; Decety and Ingvar, 1990; Denis et al., 1991; Decety et al., 1994). Most important appears the statement that at some electrode sites where such subjective responses were elicited, the stimulation at a higher current could evoke an overt motor response (Fried et al., 1991). Another explanation for the lack of a signi®cant difference between E-E and E-I might be that both tasks actually activate the same cortical areas to the same extent. However, this does not exclude the possibility that on a microscopic level patterns of neural activity differ between the two conditions. A motor program released during ISM is probably not completely inhibited somewhere on its way to the peripheral effector organs (Decety and Boisson, 1990; Decety and Ingvar, 1990; Decety et al., 1990), since ISM has repeatedly been shown to be accompanied by task-speci®c electromyographic activity (Jacobson, 1932; Wehner et al., 1984; Bonnet et al., 1997). In the present study, eye muscle activity conceivably could not be measured with EMG, but trials containing horizontal or vertical eye movements occurring during E-I or Rest were rejected in an of¯ine-analysis (Beisteiner et al., 1995). It is possible that neural structures activated during execution and imagination of a movement are similar on a central as well as on a peripheral level of the

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nervous system. A main distinction between those two states of motor behaviour might be represented by different quantitative levels of neuronal activity (Roland et al., 1980; Decety et al., 1988; Roth et al., 1996). This does not necessarily imply an inhibition of a released motor program (Bonnet et al., 1997), since motor suppression and motor imagery represent different processes (Naito and Matsumura, 1994). 4.2. Hemispheric asymmetry As in our previous study (Beisteiner et al., 1995), a left hemispheric lateralization of both motor conditions (E-I and E-E) was observed. Hemispheric asymmetry probably can be attributed to right-handedness and a verbal strategy (Hickok et al., 1996) employed by the subjects, in order to memorize the sequence of point movements (Decety, 1993), because several subjects reported the use of numbers to encode point positions on the monitor. An additional explanation for the observed left hemisphere dominance might reside in visuospatial demands of the experimental conditions, since certain visuospatial functions are located in the left hemisphere (Mehta et al., 1987; Mehta and Newcombe, 1991; Clarke et al., 1993; Cook et al., 1994; Hickok et al., 1996). A greater left hemispheric lateralization for hand modality (imagination compared with execution of a bilateral ®nger movement) (Beisteiner et al., 1995) than for eye modality (imagination compared with execution of eye movements) was observed. This means that internal simulation of bimanual movements critically involved the left hemisphere. In the present experiment, a sequence of eye movements had to be executed or to be imagined according to landmarks being visible on the computer screen throughout task execution. Subjects therefore, did not have to build up an internal representation of point positions during performance of E-I and E-E; they only had to keep in mind the sequence and the appropriate timing of four point movements. For ®nger modality on the other hand (Beisteiner et al., 1995), subjects had to mentally construct their own spatial scale of 5 points similar to the arrangement on the monitor, because the splints they wore on their ®ngers did not provide them with certain predetermined positions. Interestingly, this need to form an internal representation of spatial targets activated the left hemisphere, especially during imagination of a bilateral ®nger movement. This ®nding might be related to dif®culties of apractic patients when they have to hold in mind a representation of spatial targets of a movement, since ideomotor apraxia is often caused by lesions of the left parietal cortex (Goldenberg et al., 1986; Goldenberg, 1992; Sirigu et al., 1996; Ochipa et al., 1997). A selective impairment of mental representations of hand movements after parietal damage was recently demonstrated, with bilateral impairment after left-sided parietal lesions (Sirigu et al., 1996).

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