RESEARCH ARTICLE

Michel Guerraz Æ Jordan Navarro Æ Frederic Ferrero

Jacques Cremieux Æ Jean Blouin

Perceived versus actual head-on-trunk orientation during arm movementcontrol

Received: 8 September 2005 / Accepted: 3 December 2005 / Published online: 21 December 2005� Springer-Verlag 2005

Abstract Static roll head tilt induces bias in the trajectoryof upper limb voluntary movements. The aim of theexperiment was to investigate whether this bias isdependant on the perception of body configuration ra-ther than on its actual configuration. We used the ‘re-turn’ phenomenon as a method to produce dissociationbetween perceived and actual head tilt. Static roll headtilt in supine subjects was sustained for 15 min duringwhich subjects were periodically required to estimateverbally the tilt of their head respective to their trunkand draw, with their right index finger, straight linesaligned with their trunk. After 15 min, subjects’ headwere realigned with the trunk, and subjects continued togive verbal estimate of head position and perform themotor task. Results showed that the initial angulardeviation of the lines in the direction opposite to headtilt gradually diminished. The adaptation was noticeablewithin the first 3–5 min of tilt and subsequently dimin-ished. Verbal estimates confirmed the return phenome-non, i.e. subjects perceived their head as slowly returningtowards its neutral position after a few minutes of sus-tained tilt. When realigned with the trunk, subjectsexperienced the illusion that their head was tilted in theopposite direction to the initial head tilt and a linedeviation in the opposite direction to those made oninitial exposure was observed (after-effect). These results

indicate that the angular deviation in motor productionobserved in condition of static head tilt were largelyrelated to the perceived body configuration and there-fore favour the hypothesis that the conscious perceptionof body configuration plays a key role in organisingsensorimotor tasks.

Keywords Head tilt Æ Arm movement Æ Body scheme

Introduction

Head orientation and therefore the neck afferents thataccompany any head displacement relative to the trunkhave been shown to be determinant in the control ofvarious sensorimotor tasks. These tasks have includedwalking (Bove et al. 2004; De Jong et al. 1977), standingupright (Cohen 1961; Kavounoudias et al. 1999; Popovet al. 1996; Roll and Roll 1988), and moving the arm(Biguer et al. 1988; Blouin et al. 1998; Guerraz et al.1998; Henriques and Crawford 2002) or the eyes(Karlberg and Magnusson 1996). The early work ofCohen (1961) and of De Jong et al. (1977) have providedamong the most significant findings attesting the keyrole of the neck in the control of spatially orientedmovements. These authors showed that the injection oflocal anaesthetics in the neck in animals as well as hu-mans produced substantial sensorimotor deficits. In-deed, in their human subjects, the supposed interruptionof afferent flow from neck muscles induced ataxia,staggering gait, and hypotonia of lower and upper seg-ments, as well as sensation of falling.

Although a less dramatic effect, static head tilt in-duces bias in perceptual (Guerraz et al. 1998, 2000;Kerkhoff 1999; Luyat et al. 2001) as well as sensorimo-tor (Berger et al. 1998; Guerraz et al. 2003) processes.This has been particularly well demonstrated by Bergeret al. (1998) who investigated the consequences ofdifferent head to trunk positions on arm movementsunder normal gravity and during prolonged space flight.

M. Guerraz (&)Laboratoire de Psychologie et Neurocognition,CNRS UMR 5105, Universite de Savoie,73376 Le Bourget du lac, Chambery, FranceE-mail: michel.guerraz@univ-savoie.fr

J. Navarro Æ J. BlouinUMR Mouvement et Perception 6152,CNRS et Universite de la Mediterranee, 163 avenue de Luminy,Case Postale 910, 13288 Marseille Cedex 9, France

F. Ferrero Æ J. CremieuxLaboratoire d’Ergonomie Sportive et Performance,UFR STAPS, Universite du Sud Toulon, Var BP 132,83957 La Garde Cedex, France

Exp Brain Res (2006) 172: 221–229DOI 10.1007/s00221-005-0316-3

Subjects were required to point with the eyes closedtowards two targets previously seen presented in thehorizontal plane. Results revealed that roll head tilt in-duced a horizontal bias of the arm movements to theother side that increased in microgravity. Similar effectsof head-on-trunk position were reported by Guerrazet al. (2003) in a drawing task. Participants were re-quired to reproduce, with the eyes closed, a previouslyseen geometric shape (square or diamond). During thedrawing task, their head was either aligned with thetrunk or tilted towards the right or left shoulder. Theexperiment was conducted on earth but subjects wereeither seated upright or lying on their back (supine po-sition). It must be stressed that tilting the head in thesupine position selectively stimulates neck muscle pro-prioception without modulating vestibular signals, asthe output of the otolith organs is independent of head-on-trunk orientation in that position. Results showedthat in the seated condition, hand drawings were sub-jected to an overall rotation of a few of degrees in theopposite direction to the tilt. When supine the rotationwas three times greater than in the seated condition. Theincreased influence of head tilt on sensorimotor tasksperformed both in microgravity and on earth in thesupine posture attests the importance of head-to-neck–to-trunk relationships in the control of hand/armmovement in space.

The errors observed in both the pointing and drawingtasks during static head tilt could indicate a bias in theinternal representation of body configuration. The er-rors induced by tilting the head on the trunk, which areusually in the opposite direction to the tilt, may indicatethat subjects over-estimate the angle between their headand their trunk. Such a misperception would be partic-ularly prejudicial in impoverished sensory conditions(absence of pertinent visual or gravitational cues) inwhich the trunk constitutes the main reference to controlarm movement (Gurfinkel et al. 1993). The error indetermining the angle between the head and the trunkcould result from errors in determining the position ofeither the head or the trunk, or of both segments.

It is well known that the perception of body config-uration does not systematically coincide with its realconfiguration. For instance, keeping the head rotatedtowards the left or right shoulder during a few minuteswith the eyes closed, leads to the perception that thehead is slowly returning to its neutral position (i.e.aligned with the trunk). The perception of the head’srealignment on the trunk is called the return phenome-non (Werner et al. 1953). When the head is subsequentlyrealigned with the trunk, the subject perceives rotationin the opposite direction with respect to the initial headdeviation. Both the return phenomenon and its after-effect provide easy ways to dissociate the perception ofthe head to trunk configuration and the actual config-uration experimentally. Exploiting such a dissociationGurfinkel et al. (1992) showed, for instance, that theredistribution of the tension in limb muscles induced byhead rotation, known as a ‘‘neck reflex’’, was dependant

on the perceived rather than on the actual relation be-tween the head and the trunk. Mars et al. (1998) showedthat the perception of body straight ahead was alsodependent on perceived rather than actual head rota-tion. In the absence of visual cues, perception of straightahead is classically deviated by a few degrees in thedirection opposite to the head rotation (Biguer et al.1988). Interestingly, similar shifts occur when subjectsexperience illusory head rotation (Mars et al. 1998).Together, these results highlight the determinant role ofbody configuration perception (in Gurfunkel’s words‘‘of internal representation’’) in both motor and per-ceptual processes.

The aim of the present experiment was to investigatewhether the bias in upper limb voluntary movementspreviously observed in condition of static roll head tilt(Berger et al. 1998; Guerraz et al. 2003) is dependant onthe perception of body configuration rather than on itsactual configuration. We used the return phenomenon asa method to produce dissociation between perceptionand actual body configuration. This was achieved bysustaining static roll head tilt for a period of 15 minduring which subjects were required to perform an arm–hand motor task. Following this posture, subjects’ headwas realigned with the trunk and subjects continued toperform the task. The return phenomenon and its post-effect were quantified by asking subjects to periodicallyevaluate verbally their head to trunk angle

Methods

Subjects

Twelve healthy subjects (three females and nine males)aged 19–27 years (mean 23.2, SD 2.5) consented toparticipate. All the subjects were right handed accordingto the Edinburgh Inventory test (Oldfield 1971) and hadno history of vestibular, visual, or neuromuscular dis-ease. Informed consent was obtained prior to theexperiments according to the Declaration of Helsinki.

Procedure and apparatus

Subjects, blindfolded, lay on their back on a thin mat-tress (1 cm). A wooden board was oriented in the hori-zontal plane (fronto-parallel), 50 cm above subjects.Subjects’ heads were held aligned with the trunk or tiltedtowards the left or right shoulder by a framework whichgripped and restrained the skull.

The arm motor task

Subjects’ task was to draw straight lines of about25–30 cm on the board above them with their right in-dex finger. The lines were to be aligned with their trunk.The involvement of finger and wrist in drawing lines of

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such length has been shown to be minimal, the elbowand shoulder being the prime effectors for such move-ments (Lacquaniti et al. 1987). Nevertheless, to avoidlarge differences in the motor strategies used to draw thelines, subjects’ wrist and index finger were maintained ina fixed pointing position by a light wooden baton at-tached to the forearm and finger.

At the beginning of each trial, subjects positionedtheir index finger on the board (approximately at thelevel of their neck) and waited for a ‘go’ signal fromthe experimenter. After the signal, subjects producedfour consecutive lines in attempted alignment withtheir trunk (i.e. two return movements). The firstmovement had to be orientated towards the navel (thelower part of the board). The finger had to be con-tinuously in contact with the board. To facilitate dataanalysis, subjects were asked to keep their finger stillbriefly at the end of each line. Having completed thedrawing task, subjects removed their finger from theboard and rested their arm on their body. To ensurethat subjects produced lines of similar amplitude theexperimenter drew prior to the experiment a 25–30 cmline on a wall as an example of the average expectedlength. No constraint was given about movement time(on average, a line was produced in 700–800 ms). Nofeedback about reproduction accuracy was given dur-ing the experiment.

Subjects produced their movements approximately20 s after the experimenter moved their head to dif-ferent positions with respect to the trunk: head tilted30� towards either the left or the right shoulder orhead aligned with the trunk (0�, control condition).Three lines drawn on the mattress helped the experi-menter to reach the goal head positions (30�, 0�, and�30�). Subjects remained in these positions for 15 min.During this period, they produced their series ofmovements every minute after hearing a ‘‘go’’ signalfrom the experimenter (15 test trials). After the 15thseries, subjects’ head was returned slowly by theexperimenter in its neutral position (aligned with thetrunk in about 3–4 s). The head was maintained inthat position for 5 min during which subjects wereagain required to complete the line drawing task everyminute (five post-test trials). Each subject was tested inthe three conditions of head orientation (three blocksof 20 trials), the order of presentation of those con-ditions being counterbalanced between subjects. Theinter-block interval was 15 min to ensure dissipation ofany after-effect. During this period, subjects stood upand could move freely.

Data collection

Horizontal displacements of the right index finger wererecorded with a Polhemus 3D space Fastrak. The re-ceiver-coil of the 3D magnetic sensor was fixed on thesubjects’ fingertip. Output signals from the Fastrak weresampled at a rate of 120 Hz.

Data analysis

The effect of the head position was evaluated on twoparameters of the lines drawn by the subjects. Theseparameters were the orientation and the length of thelines. Line orientation was estimated using regressionanalyses fitting together the X–Y data points of eachindividual segment. The slope values of the linearequations were then transformed into angular measures.The number of data points varied according to the timeused to draw the lines (they varied between 80 and 150points). As can be seen in the sample trials presented inFig. 1, the segments were mostly linear. This was alsoconfirmed by the high correlation coefficient of theregression analysis found in individual segments (all r2

values were greater than 0.90). Therefore, the segmentswere well characterised by first-order regressions.According to convention, counter-clockwise angulardeviation was expressed as negative and clockwisedeviation as positive. Data were analysed using two re-peated-measures analyses of variance (ANOVAs). Atwo-way (3·15) ANOVA was carried out to test fordifferences between the three head positions [tilted left,aligned (0�), and tilted right] and the fifteen levels of thetime factor during sustained head tilt. The after-effectwas evaluated with a second two-way (3·5) ANOVAwith three post-head tilt levels (post-tilted left, post-aligned, and post-tilted right) and five time levels(immediately after return, 1, 2, 3, and 4 min after thereturn to neutral position) and time as within subjects’factors. Newman–Keuls method was used for post hoccomparisons. A 0.05 significance level was adoptedthroughout the analyses. Because the head tilt and timefactors had no significant effect on the length of thedrawing lines, only the results related to line orientationwill be presented (on average, the lines were 31.5 cmlong).

Evaluation of the return phenomenon

In order to assess the return phenomena, subjects wererequired to estimate verbally the angle between theirhead and their trunk throughout the experiment. Wenoticed in a pilot study that subjects had great difficultiesin estimating the angle in degrees between their trunkand their head [as reported previously by Darling et al.(1996)]. They largely overestimated this angle and fre-quently perceived their 30� tilted head as being tilted 45�.Therefore, in order to facilitate subject’s task, theexperimenter mentioned at the beginning of each blockof 20 trials the initial head angle relatively to the trunk(30� left, aligned, and 30� right). The purpose of theverbal estimates was to evaluate any change with time inperceived head to trunk angle, i.e. the return phenome-non. Such subjective estimates were requested every threetrials (i.e. every 3 min), after the subjects had achievedtheir drawing task. Three verbal estimates of head tiltwere also obtained during the post-test conditions; these

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were given immediately after the first, third, and fifthseries of line drawings.

The verbal estimates were also subjected to statisticalanalyses. To assess the return phenomenon, data wereanalysed using a two-way (3·5) ANOVA with the headposition [tilted left (30�), aligned (0�), and tilted right(30�)] and the time as within subject factors. The after-effect was evaluated with a second two-way (3·3)ANOVA with three post-head tilt (post-tilted left, post-aligned, and post-tilted right) and time as within subjectfactors. Newman–Keuls method was used for post hoccomparisons.

Results

The arm motor task

Effect of sustained head tilt

Results showed that the orientation of the lines wasstrongly affected by head position (ANOVA:F2,22=11.1, P<0.01). With the head straight, the ori-entation of the lines was nearly aligned with the trunk,with a mean angular deviation of 0.8� (SD=4.5�). Tilt-ing the head to the right or to the left induced an angulardeviation of the lines in the direction opposite to the tilt.The mean deviation observed during the first trial afterhead tilt (i.e. during the first minute of head deviation)was 11.85� (SD=7.76�) and –9.7� (SD=8.36�) for headtilt to the left and to the right, respectively. Figure 1

shows lines drawn with the head either straight or tiltedsideways of one subject who showed typical responses.However, as noted previously in a study using a similartask (Guerraz et al. 2003), the magnitude of thosedeviations varied largely between individuals, with aminimum of 1.2� to a maximum of 21.4� in the presentexperiment.

The magnitude of the line deviation gradually de-creased when the head remained tilted 30� towards eithershoulder (Fig. 2). This was observed in ten out of twelvesubjects. This adaptation phenomenon was confirmedby the ANOVA that showed a significant interactionbetween time and head position (F28,308=4.5, P<0.01).As shown in Fig. 2, the bias did not completely vanishedafter 14 min of head tilt and line orientations in left andright tilt conditions still significantly differed from eachother after 15 min (pair-ways comparison, P<0.05).However, they did not significantly differ anymore fromthose measured in the head straight condition after 9and 5 min after sustained head tilt to the left and to theright, respectively (P>0.05). This adaptation phenom-enon was well fitted by a log function withy=�2.71 ln(x)+12.5 (r=0.91) for left head tilt andy=2.74 ln(x)�9.2 (r=0.91) for right head tilt. Theadaptation was, therefore, particularly noticeable withinthe first 3–5 min of tilt and less evident subsequently.

Line deviation in conditions of head tilt to the rightand left were opposite in direction but otherwise sym-metrical and similarly affected by the time factor. Whenpooling responses with rightward and leftward head tilt,the mean estimates were �10.8� (SD=5.4) and �3.6�

Fig. 1 Lines produced by arepresentative subject whendrawing lines with the eyesclosed with the head eitherstraight (0�), or tilted towardsthe right (30�) or left shoulder(�30�). Each trace represents asingle trial. The y-displacementof the index is plotted againstthe x-displacement. A deviationin the opposite direction tohead tilt is apparent whencompared with the headstraight condition

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(SD=5.3) for the first and 15th trials, respectively;corresponding to a reduction of the angular bias of�67%. Figure 3 represents the mean line orientation ofpooled data as well as the logarithmic curves during the15-min period of sustained head roll tilt and also afterrealignment with the trunk (5 min).

After-effect

On return to the neutral position (head straight) after15 min of sustained head tilt, subjects exhibited an after-effect when tracing the lines. Indeed, the orientation ofthe first line after return was deviated in the oppositedirection to those made on initial exposure to head tilt(see Fig. 2). The post-effect diminished rapidly, andvanished about 3–4 min after the head return. The after-effect is confirmed by the significant interaction betweentime and post-head tilt (F8,88=4.1, P<0.01). Threeminutes after the repositioning of the head (third trial),

the line orientations were no longer different to thoseduring head straight trials (pair-ways comparisons,P>0.05).

Supplementary analyses showed that when data ob-tained in the right and left head tilt conditions werepooled (by reversing traces with post-head tilt from theleft), a modest but significant negative correlation(r=�0.58, P=0.04) was observed between the firstmeasurement after head tilt and the first one followingthe realignment of the head with the trunk. This corre-lation indicates that the greater the line deviation afterhead tilt, the greater the post-effect. For instance, sub-jects that showed greater line deviations following headtilt also showed greater deviations in the oppositedirection after head return. However, it must be notedthat such a correlation did not reach a significant levelwhen data were not pooled. We also observed that insubjects who exhibited a strong decrease in line devia-tion during sustained head tilt (as expressed by the firstcomponent of the individual logarithmic function), the

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Fig. 2 Mean segmentorientations (and standarderrors of the mean) of the 12subjects during the 15 minperiod of sustained roll head tilt(either 30� towards the left orright shoulder) and afterrealignment with the trunk(5 min). The thin line representsthe control condition with headstraight. Counter-clockwisedeviations are expressed asnegative, clockwise deviationsas positive

Post-tiltSustained head tilt

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Fig. 3 Mean line orientationsduring the 15 min period ofsustained head roll tilt and afterrealignment with the trunk(5 min) with rightward andleftward head tilt combined.Logarithmic curves for eachperiod are displayed

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after-effect also vanished quickly. This observation wasconfirmed by the significant negative correlation be-tween the first component of the log function computedfor each individual subject during the 15 min of sus-tained head tilt and the first component computed in thepost-tilt condition (r=�0.56, P=0.05).

Verbal estimate of head–trunk angle

Illusory head return and after-effect

Keeping the head passively tilted 30� towards the left orright shoulder caused most subjects to feel, after a fewminutes, that their head was slowly returning towards aneutral position (aligned with the trunk). This can beseen in Fig. 4 that shows the mean subjective estimate ofhead–trunk angle over time. Subjects estimated theirhead as being tilted by 16.9� (SD=10.1) and �19.5�(SD=9.6) after 15 min of sustained head tilt to right andleft, respectively; corresponding to approximately 40%of reduction as compared to the initial reference angle of30�. This subjective report refers to the expected ‘returnphenomenon’. This illusory head return was confirmedby a significant interaction between the head positionand time factors (F8,88=10.05, P<0.01). Two out of 12subjects did not feel any return phenomenon throughoutthe 14 min of sustained head tilt. One of those twosubjects did not show adaptation in line production.

After 15 min of sustained head tilt, subject’s head waspassively and slowly returned to the neutral position(realigned with the trunk). Immediately after this headre-alignment, the subjects felt their head tilted in theopposite direction to the previous head tilt direction.

The mean head tilt estimates were 6.9� (SD=7.4) and�6.3� (SD=6.3) when the head was returned to theneutral position from left and right head tilt, respec-tively. This after-effect diminished rapidly. This wasconfirmed by a significant interaction between post-headtilt and time (F4,44=5.7, P<0.01). All but one subjectexperienced this after-effect. However, large inter-indi-vidual differences were found as the magnitude of theafter-effect varied between 18� and 1� when measuredafter the first minute of head return.

Correlation between the drawing task and the verbalestimate

Most subjects showed a net adaptation to sustainedhead tilt in the motor task that was concomitant with anillusion that their head was slowly returning towards itsneutral position but no significant correlation could bebetween these two phenomena. However, a negativecorrelation was noted between the amplitude of head tiltillusion following the repositioning of the head from theleft side to neutral position and the line drawing task inthat condition (r=�0.69, P<0.05). Therefore, the morethe head was perceived as tilted after physical realign-ment the greater were the line deviations in the oppositedirection. Such a significant correlation was not ob-served when the head was returned from the right side.

Discussion

In the present experiment, supine subjects were requiredto draw lines aligned with their trunk in the fronto-

Sustained head tilt Post head tilt

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Fig. 4 Mean verbal estimates (and standard errors of the mean) ofthe 12 subjects of head to trunk angle during the 15 min period ofsustained roll head tilt (either 30� towards the left or right shoulder)and after realignment with the trunk (5 min). The thin linerepresents the control condition with head straight. The black,grey and white circles represented on the ordinate axis correspond

to the reference values (�30�, +30�, 0�) given to the subjects at thebeginning of each block of 20 trials. In the sustained periods, verbalestimates were systematically made relatively to these referencevalues and therefore traduce any perceived change with time in theangle between the head and the trunk

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parallel plane with and without sustained head tilt. Thelines produced just after tilting the head were subjectedto a large angular deviation in the direction opposite tohead tilt. This head tilt effect gradually vanished andreached a plateau after 8–10 min. Thereafter, line ori-entation remained deviated from the trunk midline byabout 3–5�. When the head was realigned with the trunk,an after-effect appeared. This effect, which consisted of aline deviation in the opposite direction to those made oninitial exposure to head tilt, disappeared within 3–5 min.Throughout the experiment, subjects were also requiredto estimate verbally any perceived change in their headposition relative to their trunk. As expected, subjectsexperienced the return phenomenon, i.e. the feeling thatthe head was slowly returning towards its neutral posi-tion after a few minutes of sustained tilt. Consequently,when the head returned to the neutral position, subjectsexperienced the illusion that their head was tilted in theopposite direction to the initial head tilt.

The angular deviation provoked by static head tilt inthe task of drawing segments aligned with the trunkindicates that, at least within the few minutes followinghead tilt, the angle between the head and the trunk maybe over-estimated by the CNS. This is in agreement withobservation in pilot studies in which subjects had greatdifficulties in estimating the angle in degrees betweentheir trunk and their head (as reported previously byDarling et al. 1996) and overestimated this angle (seeMethods). The trunk being an important frame of ref-erence to plan and control movements, any bias in thisreference system would have a significant impact onhand–arm motor tasks. Accordingly, the angular devi-ations reported in sensibly different, externally oriented,motor behavior such as pointing (Berger et al. 1998) anddrawing reproduction (Guerraz et al. 2003) are probablythe indirect witness of such over-estimate of head totrunk angle. In other words, asking subjects to pointtowards, or reproduce, previously seen objects in theabsence of actual extrinsic references (visual or gravita-tional cues) could be seen as a way to implicitly deter-mine subjects’ perception of trunk orientation, what wasexplicitly required in the present experiment. The errorsin estimating either explicitly or implicitly the trunkorientation in the above-mentioned tasks may indicatethat the CNS has great difficulties in correctly comput-ing different head to trunk configurations, on the basisof neck muscle proprioception alone (neither visual norvestibular cues being available in our experiment). Atfirst glance, this is hardly compatible with the extraor-dinary ability of the CNS to integrate neck afferents incomplex motor tasks such as eye–head–hand movements(Becker and Saglam 2001; Blouin et al. 1998, 1999;Henriques and Crawford 2002; Henriques et al. 2003) orpostural control (Gurfinkel et al. 1988; Kavounoudiaset al. 1999; Lund 1980; Thurrell et al. 2000). However,while the CNS is highly efficient at encoding anddetecting relative changes on the basis of sensorial cues,it appears not so well equipped and informed aboutabsolute references. For instance, Mergner et al. (1991)

reported that in condition where the trunk is rotated atlow frequencies with the head kept stationary—stimu-lating neck receptors solely—subject’s estimates ofrotation magnitude is erroneous with a gain largely be-low 1. In contrast, the detection threshold of angularhead rotation (neck stimulation) in the absence of ves-tibular stimulation was rather low (velocity threshold of1�/s). Considering the characteristics of muscle spindles,one can expect a discrepancy between relative andabsolute estimates. Indeed, the Ia fibres and also, but toa much lesser extent, the II fibres (mainly known as tonicfibres) have adaptive properties and therefore providethe CNS with changing signal over time. Giving priorityto changes, the CNS does not track unchanging infor-mation so well. The return phenomenon highlights theseadaptative processes.

Whilst acknowledging the adaptive characteristics ofmuscle spindles, Gurfinkel et al. (1992) suggested thatthe return phenomenon was mainly due to some sort of‘‘drift’’ in the internal representation of prolonged bodyconfigurations. As suggested by Merleau-Ponty (1945),the internal model of the body (body scheme) is notsimply the result of association of kinaesthetic cues(sensory afferents) but rather a framework in whichthese cues are synthesised on the basis of internal rep-resentations. The ‘‘phantom limbs’’ often reported byamputees attest that the representation of body config-uration is partly independent on afferent cues.

The present experiment was designed to establishwhether the angular deviation of arm–hand motor pro-ductions observed in conditions of static head tilt weredependent on the perceived body configuration or actualbody configuration. As expected, exposing subjects tosustained head tilt produced dissociation between per-ceived and real head tilt on two occasions: first, afterseveral minutes of sustained head tilt (return phenome-non) and second, when the head was returned to itsneutral position (after-effect—illusion of tilt). On bothoccasions, the average orientations of lines drawn by thesubjects were related to the average perceptual estimates.Indeed, the time course of improvement in the motortask (i.e. line orientations returning towards trunk ori-entation) was simultaneous with the return phenome-non. Even more, the illusion of head tilt on return to theneutral position was accompanied by the reappearanceof motor deviations in the opposite direction to theillusory tilt. Therefore, these results attest that theangular deviation observed in the task of drawing linesaligned with the trunk are to some extent related to theperceived body configuration.

The results of the present experiment closely matchthe observation of Gurfinkel et al. (1991, 1992) onpostural automatisms referred to above. They are alsoconsistent with the observations of Mars et al. (1998) onbody straight ahead estimates during prolonged headrotation in yaw. Mars et al. (1998) failed to show asignificant impact (they found a tendency) of sustainedhead rotation (in yaw) on the shift in the straight aheadpointing movements. However, interestingly, when

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subject’s head was realigned with the body after 9 min ofsustained rotation, they experienced an illusory rotationof their head by �15� in the opposite direction to theinitial rotation. At the same time, they exhibited a shiftof body midline estimates contralaterally to this ‘‘per-ceived’’ head position. Therefore, motor estimates ofboth body straight-ahead (translation error) and trunkorientation (rotation error) seem to be intimately linkedto the perceived body configuration rather than to thereal configuration.

However, a close inspection of the present resultsrevealed some discrepancies between the motor task andthe perceptual estimates. Indeed, lines deviationsdiminished by �67% during the 15 min of sustainedhead tilt, and were no more significantly different after8–10 min from those observed with head straight. Incontrast, the return phenomenon was more modest(�40%) and followed a more linear trend. Moreover, nosubject reported after 15 min of sustained head tilt tofeel his head as being aligned with his trunk. In addition,correlation analysis failed to show systematic correlationbetween the two phenomena. One explanation of thosediscrepancies might stem from the fact that subjects hadthe explicit knowledge that their head was locked in atilted position. This knowledge could limit or interferewith the return phenomenon and as a consequence re-duce the link between those two phenomena. Addi-tionally, the fact that the line production and perceptualestimates were investigated every minute and every3 min, respectively, also might reduce the statisticalpower of our analysis. Another explanation, diametri-cally opposite, would be that the two phenomena followthe same general trend but are in fact independent. Thiswould invalidate our main hypothesis according towhich voluntary movements performed in condition ofstatic roll head tilt are to some extent dependant on theperception of body configuration. With respect to theabove-mentioned work of Gurfinkel et al. (1992) andMars et al. (1998) such an explanation seems unlikely. Inaddition, the hypothesis of independent motor andperceptual processes is not supported by the significantcorrelation, we found between the perceived position ofthe head after realignment with the trunk (after sus-tained left head tilt) and the line deviations. Indeed, thiscorrelation indicated that the more subjects perceivedtheir head tilted after having been realigned with thetrunk, the greater their lines were deviated in theopposite direction.

In overview, these results confirm that internalrepresentation of body configuration (the body scheme),giving rise to the conscious perception of body config-uration, is an important actor playing key role inorganising sensorimotor tasks, such as drawing geo-metric figures (Guerraz et al. 2003) and pointing towardsremembered targets (Berger et al. 1998). This actor,highly sensitive to dynamic cues, would be fit to subservethe integration of new movements or postures (seeHaggard and Wolpert 2005). The downside of its‘‘alertness’’ to any fresh information probably renders it

less well appropriate to evaluating static postures such assustained head tilt, which therefore leads to biases in theperception of body configuration and dependent motortasks.

Acknowledgements This work was supported by the Universite duSud Toulon-Var and was conducted at the Laboratoire d’Ergon-omie Sportive et Performance (UFR STAPS). The authors aregrateful to Pr. M. Gresty and Dr. R Reynolds for their Englishsupport.

References

Becker W, Saglam H (2001) Perception of angular head positionduring attempted realignment with eccentric visual objects. ExpBrain Res 138:185–192

Berger M, Lechner-Steinleitner S, Kozlovskaya I, Holzmuller G,Mescheriakov S, Sokolov A, Gerstenbrand F (1998) The effectof head to trunk position on the direction of arm movementsbefore, during, and after space flight. J Vestib Res 8:341–354

Biguer B, Donaldson IML, Hein A, Jeannerod M (1988) Neckmuscle vibration modifies the representation of visual motionand direction in man. Brain 111:1405–1424

Blouin J, Okada T, Wolsley C, Bronstein AM (1998) Encodingtarget–trunk relative position: cervical versus vestibular con-tribution. Exp Brain Res 122:101–107

Blouin J, Amade N, Vercher J-L, Gauthier GM (1999) Opposingresistance to the head movement does not affect space percep-tion during head rotation. In: Becker W, Deubel H, Mergner T(Eds) Current oculomotor research: physiological and psycho-logical aspects, Plenum, London, pp 193–201

Bove M, Brichetto G, Abbruzzese G, Marchese R, Schieppati M(2004) Neck proprioception and spatial orientation in cervicaldystonia. Brain 127:2764–2778

Cohen LA (1961) Role of eye and neck proprioceptive mechanismsin body orientation and motor coordination. J Neurophysiol24:1–11

Darling WG, Butler AJ, Williams TE (1996) Visual perceptions ofhead-fixed and trunk-fixed anterior/posterior axes. Exp BrainRes 112:127–134

De Jong PTVM, De Jong JMBV, Cohen B, Leonard B, JongkeesLB (1977) Ataxia and nystagmus induced by injection of localanesthetics in the neck. Ann Neurol 1:240–246

Guerraz M, Poquin D, Ohlmann T (1998) The role of head centricspatial reference with static and kinetic visual disturbances.Percept Psychophys 60:287–295

Guerraz M, Luyat M, Poquin D, Ohlmann T (2000) The role ofneck afferents on subjective orientation in the visual and tactilesensory modalities. Acta Otolaryngol 120:735–738

Guerraz M, Blouin J, Vercher J-L (2003) From head orientation tohand control: evidence of both neck and vestibular involvementin hand drawing. Exp Brain Res 150:40–49

Gurfinkel VS, Levik YS (1991) Perceptual and automatic aspects ofthe postural body scheme. In: Paillard J (Ed) Brain and space,Oxford University Press, Oxford, pp 147–162

Gurfinkel VS, Levik YS, Popov KE, Smetanin BN, Shilkov YV(1988) Body scheme in the control of postural activity. In:Gurfinkel VS, Ioffe ME, Massion J, Roll JP (Eds) Stance andmotion, Plenum, New York, pp 185–193

Gurfinkel VS, Lebedev MA, Levick YS (1992) What about the so-called neck reflexes in humans ? In: Berthoz A, Graf PW, VidalPP (Eds) The head–neck sensory motor system, Oxford Uni-versity Press, Oxford, pp 543–547

Gurfinkel VS, Lestienne F, Levik YS, Popov KE, Lefort L (1993)Egocentric references and human spatial orientation in micro-gravity: body centred coordinates in the task of drawing ellipseswith prescribed orientation. Exp Brain Res 95:343–348

Haggard P, Wolpert DM. Disorders of body scheme. In: Freund J,Jeannerod M, Hallet M, Leiguarda R (Eds) Higher-order dis-orders. Oxford University Press (in press)

228

Henriques DYP, Crawford JD (2002) Role of eye, head, andshoulder geometry in the planning of accurate arm movements.J Neurophysiol 87:1677–1685

Henriques DYP, Medendorp WP, Gielen CC, Crawford JD (2003)Geometric computations underlying eye–hand coordination:orientations of the two eyes and the head. Exp Brain Res152:70–78

Karlberg M, Magnusson M (1996) Asymmetric optokinetic after-nystgamus induced by active or passive sustained head rota-tions. Acta Otolaryngol 116:647–651

Kavounoudias A, Gilhodes JC, Roll R, Roll JP (1999) From bal-ance regulation to body orientation: two goals for muscleproprioceptive information processing? Exp Brain Res 124:80–8

Kerkhoff G (1999) Multimodal spatial orientation deficits in left-sided visual neglect. Neuropsychologia 37:1387–1405

Lacquaniti F, Ferrigno G, Pedotti A, Soechting JF, Terzuolo C(1987) Changes in spatial scale in drawing and handwriting:kinematic contributions by proximal and distal joints. J Neu-rosci 7:819–28

Lund S (1980) Postural effects of neck vibration in man. Experi-entia 36:1398

Luyat M, Gentaz E, Corte TR, Guerraz M (2001) Reference framesand haptic perception of orientation: body and head tilt effectson the oblique effect. Percept Psychophys 63:541–554

Mars F, Honore J, Richard C, Coquery JM (1998) Effects of anillusory orientation of the head on straight-ahead pointingmovements. Curr Psychol Cog 17:749–762

Mergner T, Siebold C, Schweigart G, Becker W (1991) Humanperception of horizontal trunk and head rotation in spaceduring vestibular and neck stimulation. Exp Brain Res 85:389–404

Merleau-Ponty M (1945) Phenomenologie de la perception. Gal-limard, Paris

Oldfield RC (1971) The assessment and analysis of handedness: theEdinburgh inventory. Neuropsychologia 9:97–113

Popov K, Lekhel H, Bronstein AM, Gresty MA (1996) Posturalresponses to vibration of neck muscles in patients with unilat-eral vestibular lesions. Neurosci Lett 214:202–204

Roll JP, Roll R (1988) From eye to foot. A proprioceptive chaininvolved in postural control. In: Amblard B, Berthoz A, ClaracF (Eds) Posture and gait. Elsevier, Amsterdam, pp 155–164

Thurrell A, Bertholon P, Bronstein AM (2000) Reorientation of avisually evoked postural response during passive whole bodyrotation. Exp Brain Res 133:229–232

Werner H, Wapner S, Bruell JH (1953) Experiments on sensory-tonic field theory of perception. VI. Effect of position of head,eyes, and of object on position of the apparent median plane. JExp Psychol 46:293–299

229