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Head orienting contributes to the directional accuracy of aiming at distant targets
Human Movement North-Holland
359
Science 5 (1986) 359-371
HEAD ORIENTING CONTRIBUTES TO THE DIRECTIONAL ACCURACY OF AIMING AT DISTANT TARGETS R. ROLL * Luhoraioire
de Neurosciences
C. BARD LuvcrlUniuersity,
Fonctionelles,
Marseille,
France
Marseille,
France
Quebec, Canada
J. PAILLARD Luboratoire
de Neurosciences
Fonctionelles,
Roll, R., C. Bard and J. Paillard, 1986. Head orienting contributes to the directional accuracy of aiming at distant targets. Human Movement Science 5, 359-371.
The aim of this study was to evaluate the contribution of head orienting to the directional accuracy of aiming at targets of different eccentricities. Six right-handed females were tested in three experimental conditions: (1) aiming at a target with head fixed, (2) aiming with head free to move, (3) aiming with instruction to align head with target. For all conditions, accuracy is reduced when aiming at the more eccentric targets. However, undershooting increases considerably when the head is fixed. The present results support a twofold hypothesis for encoding spatial information of visual origin: an eye ( ~15’ of eccentricity) and a head ( > 25” of eccentricity) range. It can be concluded that head movements contribute to accuracy of aiming at targets located beyond 20’ of eccentricity of the subject’s visual field, thus providing the arm program with directional specifications.
The head, as carrier of the most important captors for distant information, is the leading segment for behavioral activities. Head movements are required for orienting these captors toward sources located in extracorporeal space. In addition, the head contains the labyrinthine apparatus that allows the body to maintain its erect posture with reference to the direction of gravitational force. Changing * Requests for reprints should CNRS, Marseille, France.
0167-9457/87/$3.50
be sent to R. Roll, Laboratoire
0 1987, Elsevier Science Publishers
de Neurosciences
B.V. (North-Holland)
Fonctionelles,
360
R. Roil et al. / Heud orienting,
drrectionul
uccurrrcy, aimrng tusks
postures and movements of the body are organized with reference to head position and head movement. Thus the head, with the combined contribution of visual and vestibular information, is the main agent for the steering of spatially oriented behavior. Steering, however, presupposes a space coordinate system and some invariant or predictable features that allow programmed motor activities to be triggered and guided by visual cues in extracorporeal space. The spatial encoding of visual cues relies heavily on proprioceptive signals of several origins: fovea1 acquisition of the visual target in the retinal coordinate system has to be plotted within the head-centric coordinate system by taking into account both proprioceptive information from extraocular musculature about eye position in the orbit and proprioceptive information of labyrinthine origin about head position in the gravitational field. Finally, the evaluation of body position in relation to head position, that derives from neck proprioceptive information, allows the spatial encoding of the location of a visual target within a body-centric system of coordinates. Hand pointing at a visual target located in the near space of prehension has been extensively studied (reviewed in Paillard and Beaubaton (1978)). If the subject fixates the target, the foveation process is so precise that the directional accuracy of the pointing program of the arm is assumed to depend mainly on the calibration of eye position in the head. Both proprioceptive information from ocular muscle and efferent command of eye movements are presumed to play a role. Provided that vision of arm movement is precluded (the openloop condition excluding corrective feedback of the on-going movement), the accuracy of the pointing movement is taken to reflect the accuracy of the spatial encoding of target position. The coordinated pattern of eye and head movements that is observed when a subject directs his gaze toward a target in an unexpected eccentric position in the visual field is well known. The final gaze orientation has been shown to be independent of neck proprioceptive information provided that the vestibular system is intact (Bizzi 1980). In contrast, the directional accuracy of arm pointing is heavily affected after cervical dorsal root section in monkey (Cohen 1961); and in man, the accuracy of pointing has been shown to be improved when the head is free to move when compared with the head-fixed condition (Roll 1974; Conti 1975; Roll 1976; Marteniuk 1978; Roll et al. 1981; Biguer 1981; Biguer et al. 1984).
R. Roll et al. / Head orientrng,
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accuracy, uimmg tusks
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Previous studies have shown that the combination of head and eye movements varies with stimulus eccentricity and predictability of target position. Depending on the authors, the eccentricity of the target at which head turning accompanies eye movement varies form 10-15” (Legrand 1952; Crawford 1960) to 35-40” (Mackworth and Mackworth 1958; Bartz 1966). The functional contribution of head orienting to the overall behavioral performance obviously requires clarification (Paillard 1971). This study aims at analyzing the role of head orientation in the localization of a distant target within a body-centric space coordinate system. An aiming task has been used in preference to a classical pointing task for two reasons. (1) Distance coding is thus eliminated as a source of variance in accuracy of the performance. (2) The feedforward programming of the aiming task is presumed to be better tuned than that of a pointing task. In fact, the latter accommodates a rather large margin of inaccuracy within the triggered program of reaching, owing to the remarkable proficiency of visual feedback which assists the on-going movement especially (but not exclusively) during its terminal phase. In contrast, the accuracy of aiming at a distant target is poorly related to corrective feedback of visual origin and therefore relies, even in conditions when vision of the field of action is normal, mainly on the pretuning of the program for positioning the arm in the right orientation. Thus, precluding vision of arm movement should affect aiming less than pointing. Recent studies have shown that aiming and reaching may well rely on two different classes of the preprogramming process that are separately involved in the reorganizational process following prismatic displacement of the visual field (Rip011 1980) and that are selectively affected by pathology according to the locus of the lesion (Brouchon et al. 1980). In order to evaluate the contribution of head orienting to the directional accuracy of aiming, we measured the latter when position of the targets was randomly varied in the visual hemifield ipsilateral to the moving arm and when head constraints were varied. Furthermore, the basic assumption was that each of the body segments concerned - eye, head and trunk - has an optimal working zone at different degrees of eccentricity in the visual field. Accordingly gaze direction can be accurately defined by the calibration of the position of the eye in the orbit within a range of rotation up to 15 O. For gaze direction involving rotation of the eye above 20” of eccentricity, head
362
R. Roll et al. / Heud orienting,
drrectionul
nccuruq.
uiming
task3
rotation would automatically be implicated to bring back the eye within its optimal calibrating range. Then, head-trunk calibration could obey similar boundary constraints at about 40” of eccentricity where a rotation of the shoulder girdle would be required to allow for better calibration of the relative positions of head and trunk. With these considerations in mind, we specified three zones of eccentricity and treated the data accordingly.
Method
Subjects Six right-handed females, aged 25-35, participated as paid subjects. All were tested in three experimental conditions: (1) aiming at the target with head fixed, (2) aiming with head free to move, (3) aiming with instructions to align head with target.
Apparatus The subject was seated with trunk restrained by a seat belt and facing a semi-circular wooden board (180 cm height, 110 cm radius) on which 19 light-emitting diodes (LED) were displayed horizontally at the level of the subject’s eyes. The LEDs were located 9.65 cm apart, subtending a 5” visual angle with respect to the subject’s position. They covered a total visual field of 90”. For biomechanical reasons only targets in the right hemifield were used. In all conditions the subject wore a head-helmet topped by a spot-light designed to project a small luminous arrow on the squared paper covering of the semi-circular panel. Also, she held in her hand another spot-light, identical to the first one but projecting a smaller arrow, with which she points at the target (fig, 1). For each trial the projection on the target of the head and hand spot-lights was photographed with a camera (Olympus 0M2) placed above the subject’s head. In addition, a wooden board was placed horizontally underneath the subject’s chin, to prevent her from viewing either her hand move-
R. Roll ei al. / Head orienting, directionul accumcy, aiming tusks
Fig. 1. Experimental
set-up.
A - frontal
363
view; B - top view.
ment or the pointing error on the panel. A chin-rest was mounted on the board for conditions in which the head was restrained. Procedure Subjects were seated in a dimly lit room with both hands resting on their knees, holding a spot-light in their right hand. They were instructed to keep eyes and head facing straight in front of them, thus gazing at the illuminated central diode. Under all experimental conditions and before and after each aiming movement, they had to maintain this resting position and to fixate the central diode until another peripheral target was presented. Then subjects had to direct, as accurately as possible, their spot-light toward the just illuminated target by stretching their arm at full length from the resting position of the hand
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directional
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tasks
on the knee and to stabilize the spot-light in that direction until the experimenter had made a photograph of the screen and instructed the subject to resume the resting position. No instructions were given concerning the speed of movement execution. Subjects were performing at their spontaneous self-pacing rate (usually in the range of movement time of about 500 msec). They had, however, undergone a training session during which they were allowed to see the projection of their spot-light on the screen and thus to evaluate and correct their aiming error. All subjects performed in three experimental conditions (head constraints): head free to move; head restrained by a chin-rest; and head aligned on target. Each condition involved a total of fifty-four randomly presented trials (9 targets x 6 trials). The targets were located from 5” to 45” of eccentricity, five degrees apart, in the subject’s right hemifield. The picture photographed of each trial against millimetric squared paper on the viewing screen provided a direct and precise recording of head and hand directional errors relative to target position. Differences in size and pattern of the spot-lights on head and arm allow their easy identification on each picture. The results in accuracy of aiming were collapsed within three target zones in accordance with our initial hypothesis: zone 1 included targets of 5”, 10” and 15” of eccentricity; zone 2 included targets of 20”, 25” and 30”, and zone 3 targets of 35”, 40” and 45” of eccentricity. Accuracy was evaluated from three scores: the absolute error, the constant error, and the variable error. Analyses of variance (3 head conditions X 3 zones), with repeated measures on each factor, were applied to each dependent variable.
Results (1) For absolute error, no significant difference was found for the main factors, however, the interaction head/zone was significant F(4, 20) = 2.87, p = -c 0.05, showing an increase of error according to target eccentricity in the head-fixed condition (fig. 2). (2) For constant error, the analysis revealed a significant head condition effect, F(2, 10) = 4.94, p < 0.03; a Duncan post hoc analysis showed that the head-fixed condition significantly differed from the
R. Roll et al. / Head orienting,
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accurrrcy, aiming
tasks
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head fixed
3-
I
I
3
1
Z&E
Fig. 2. Absolute
spatial
error according
to head condition
and target zone.
other two conditions (fig. 3). In addition, there was a significant effect of angular zone, F(2, 10) = 13.52, p < 0.01; a Duncan post hoc analysis revealed a significantly larger undershooting in zone 3 than in both other zones. (3) For variable error, no significant difference was found for any of the main factors.
Discussion For all head conditions, accuracy is reduced when aiming at the more eccentric targets. However, undershooting increases considerably when the head is fixed. The hypothesis that man would rely on two modes of encoding spatial information of visual origin provides a possible interpretation of the present results. It seems that up to 15 o of
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head +
position fixed
-+-lined
Fig. 3. Constant
spatial
error according
to head condition
up
and target zone
eccentricity, the arm movement programming is based upon information from the eye-in-head position, mainly computed from saccade amplitude. Prablanc and Biguer (1982) who did not find a significant correlation between hand and eye error, claimed that the efferent copy of the saccade could be used for initiating, rather than computing, the aiming movement. However, as recently suggested by Roll and Roll (1986), the possible influence of proprioceptive extraretinal signal from stretched eye muscles for evaluating the eye-in-head position can not be ruled out, especially as both head and trunk are fixed. The second mode of encoding relies on additional information coming from head position with respect to the trunk and operates beyond 20” of eccentricity, when head movement is systematically associated with eye displacement. Paillard (1976) already suggested that head-position cues would be taken into account in the programming of an arm trajectory at the target, and might contribute to the directional specification within the program of reaching. The head contribution to
R. Roll et al. / Head orienting, directiorml crccuracy, aiming tusks
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reaching accuracy in slow movements has also been demonstrated by Marteniuk (1978). Thus, a twofold hypothesis for coding is supported by both psychophysiological and neurophysiological data. First, a 15” range is considered as the eye ‘working zone’ (Dodge and Cline 1901; Lancaster 1941). It seems to correspond to a significant value for the oculomotor system, whatever the task to be performed. Bahill et al. (1975) showed that most saccades occurring in natural circumstances reach 15” of eccentricity in man. Second, Biguer et al. (1982; 1984) found a significant difference, beyond 30”, between head-free and head-fixed conditions in an open-loop pointing task. Moreover, the study of temporal organization of head-eye-hand coordination during reaching showed that the neck EMG activity always precedes the eye movement for eccentricities of 20”, 30” and 40”. In the head-fixed condition, the target position is undershot for all angular zones and the error increases as the target eccentricity increases. These results can be considered in relation to neurophysiological data from cat (Blakemore and Donaghy 1980; Roucoux and Crommelink 1980; Straschill and Schick 1977; Harris 1980), and monkey (Wurtz and Albano 1980). These authors indicated two modes of eye-head coordination when stimulating the superior colliculus. With respect to the region of stimulation, small amplitude saccades ( < 20-25”) without head movement, or larger saccades, were observed. If we compare the accuracy of aiming in head-free and head-aligned conditions, it is worth noticing that the most accurate aiming is achieved at 20-30” in the head-centered condition, whereas below this limit the target is overshot; conversely it is undershot beyond 30”. This result brings further evidence to the previous interpretation concerning the eye/head trade-off in the coding of visuo-spatial information according to stimulus eccentricity. Mobilization of the head is not required for small eccentricities (eye range); it leads to an overshoot of the target. The undershooting observed beyond 30” would be the result of shoulder immobilization. Conversely, in the absence of precise instruction concerning head position, namely in the head-free condition, head movements tend to bring the eye back to its working zone, without necessarily centering the head accurately on target. Biguer and Prablanc (1981) claimed that, during gaze orientation toward a visual target, the final head position does not exceed 60% or 70% of target eccentricity. In fact, head movements can be observed, even for small
368
R. Roil et (11./ Heud orienting, directional accuracy, aiming tusks
Fig. 4. Head-movement
amplitude
of eye and head movers,
according
to target eccentricity.
target eccentricities, according to a typology of individual differences which differentiates between eye and head movers. Such a distinction was introduced by Afanador and Aitsebaomo (1982) in a study of the effects of wearing progressive bifocal spectacles on the normal patterns of eye movement for near visual tasks. They observed that in normal subjects head movements sometimes occur for peripheral stimuli presented as little as two degrees away from the midline. Systematic study on 50 subjects of the range of eye movement before the head moved at least two degrees led to the division of the population into two extreme subgroups: the eye movers who exhibit ranges of eye movement exceeding 20” before moving their head; and the head movers who show ranges of less than 10” before head movement. For example, fig. 4 clearly shows that, for all target eccentricities in the right hemifield, two types of head mobilization can be observed. For eye movers, no head movement is observed up to 15”. From then on, head movement slowly increases in amplitude, and two plateaus are identified: at 25” (head range), and at 35” (shoulder range). Conversely, for head movers, the amplitude of head movement is more important. In fact the head is nearly lined up with the target for all eccentricities. Although these behavioral data might not constitute definitive evidence for the mechanisms involved, they suggest taken in conjunction with the literature on
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the informative role played by neck proprioception, that head movements are part of the aiming program according to target location. Longet (1845) described a ‘cervical ataxia’ syndrome following neck muscle lesions. Cohen’s (1961) results emphasized the role played by the neck proprioceptive receptors over the vestibular contribution in accuracy of movements from a static position. Finally, the existence of a very important pool of neuromuscular receptors in the dorsal neck muscles (Abrahams 1977) suggests a functional role for these receptors in eye/head rotation. Finally experimental support for the influence of cervical proprioception is provided by the chronological analysis of eye/head-hand coordination when a target of more than 15” of eccentricity is presented in the subject’s visual field (Biguer 1981). It was observed that the final head position is reached about 200 msec before the arm final position at the target. This delay could be sufficient to allow a program amendment on the basis of neck proprioceptive feedback, even in an open-loop condition. From the present results, it can be concluded that head movements contribute to the accuracy of aiming at targets located beyond 20” of eccentricity in the subject’s visual field (zone 2). This mechanism should bring the eye back to its optimal working zone. Head position cues could thus be considered in the programming of arm trajectories, specially for directional specifications of eccentric targets. The large undershooting observed in zone 3 may suggest that the accuracy of aiming at target beyond 40” would require the rotation of the shoulder girdle in order to bring the head back within its usual working zone.
References
Abrahams, J.C., 1977. The physiology of neck muscles: their role in head movement and maintenance of posture. Canadian Journal of Physiological Pharmacology 55, 332-338. Afanador, A.J. and P. Aitsebaomo, 1982. Contribution of eye and head movement for a near task. American Journal of Optometry and Physiological Optics 59, 863-869. Bahill, A.T., D. Adler and L. Stark, 1975. Most naturally occurring human saccades have magnitudes of 15 degrees or less. Investigative Ophthalmology 14, 468-469. Bartz, A.E., 1966. Eye and head movements in peripheral vision: nature of compensatory eye movements. Science 152, 1644-1645. Biguer, B., 1981. Coordination visuo-motrice: sequence d’activation et contrale des mouvements visuellement guides. These IIIe Cycle, Universite Lyon I.
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dtrectmml
uccurrtcy, rrirning tusks
Biguer, B. and C. Prablanc, 1981. ‘Modulation of the vestibulo-ocular reflex in eye-head orientation as a function of target distance in man?’ In: A. Fuchs and W. Becker (eds.), Progress in oculomotor research. New York: Elsevier. pp. 525-530. Biguer, B., M. Jeannerod and C. Prablanc, 1982. The coordination of eye, head and hand movements during reaching at a single visual target. Experimental Brain Research 46, 301-304. Biguer, B., C. Prablanc and M. Jeannerod, 1984. The contribution of coordinated eye and head movements in hand pointing accuracy. Experimental Brain Research 55, 462-469. Bizzi, E., 1980. ‘Central and peripheral mechanisms in motor control’. In: G.E. Stelmach and J. Requin (eds.), Tutorials in motor behavior. Amsterdam: North-Holland. pp. 131-143. Blakemore, C. and M. Donaghy, 1980. Coordination of head and eyes in the gaze changing behaviour of cats. Journal of Physiology 300, 317-335. Brouchon, M., P. Jordan and R. Roll, 1980. Behavioral space organization in man. Balint’s syndrome revisited. Film 16 mm couleur, 25 mn. CNRS, Marseille. Cohen, L.A., 1961. Role of the eye and neck proprioceptive mechanisms in body orientation and motor coordination. Journal of Neurophysiology 24, l-11. Conti, P., 1975. Parametres visuels et posturaux des coordinations visuo-matrices. Resultats preliminaires dans une t&he de pointage chez l’homme. Memoire de DEA Sciences du Comportement. Universite Aix-Marseille II. Crawford, A., 1960. The perception of moving objects. III. The coordination of eye and head movements. Flying Personnel Res. Corn. Memo.. 150 c., 14 p, Dodge, R. and T.S. Cline, 1901. The angle velocity of eye movements. Psychological Review 8, 145. Harris, L.R., 1980. The superior colliculus and movements of the head and eyes in cats. Journal of Physiology 300, 367-391. Lancaster, W.B., 1941. Fifty years experience in ocular motility. American Journal of Ophthalmology 24, 485. Legrand. Y., 1952. Optique physiologique (2e ed.). Edition de la revue d’optique. Tome III: L’espace visuel. Paris: Dunod. Longet, M., 1845. Sur les troubles qui surviennent dans l’equilibration, la station et la locomotion des animaux apres la section des parties molles de la nuque. Gazette Medicale de Paris 13. Mackworth, J.F. and N.H. Mackworth, 1958. Eye fixations recorded on changing visual scenes by the television eye marker. Journal of the Optical Society of America 48, 439-445. Marteniuk, R.G., 1978. ‘The role of eye and head positions in slow movement execution’. In: GE. Stelmach (ed.), Information processing in motor control and learning. New York: Academic Press. pp. 2677288. Paillard, J., 1971. Les determinants moteurs de l’organisation de l’espace. Cahiers de Psychologie 14 (4) 261-316. Paillard, J., 1976. Espace visuel et programmation motrice. Cahiers de Psychologie 19 (3-4). 171-180. Paillard, J. and D. Beaubaton, 1978. ‘De la coordination visuo-motrice a l’organisation de la saisie manuelle’. In: H. Hecaen et M. Jeannerod (eds.), Du contrBle de la motricite a l’organisation du geste. Paris: Masson. pp. 225-260. Prablanc. C. and B. Biguer, 1982. ‘Eye-head-hand coordination’. In: A. Roucoux and M. Crommelink (eds.), Physiological and pathological aspects of eye movements. The Hague/Boston, MA/London: D.W. Junk. pp. 431-441. Ripoll. H., 1980. Analyse comparte de coordinations visuo-manuelles de prehension et de projection. These doctorat de IIIe cycle en neuropsychologie et neurolinguistique. Paris, E.H.E.S.S. Roll, R., 1974. R81e des mouvements de la t&e dans l’indexation spatiale des donnees visuelles au tours de l’ontogenese. Memoire de DEA Sciences du Comportement, Universite An-Marseille.
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Roll, R., 1976. RfYe des mouvements de la t&e dans la coordination visuo-motrice chez l’enfant. Cahiers de Psychologie 19, 207. Roll, J.P. and R. Roll, 1986. ‘Kinaesthetic and motor effects of extraocular muscle vibration in man’. In: J.K. O’Reagan and A. Levy-Schoen (eds.), Eye movements: from physiology to cognition. Edited Proceedings of the Thud European Conference on Eye Movements, Dourdan, France 1985. Amsterdam: North-Holland. Roll, R.. C. Bard and J. Paillard, 1981. Rale des mouvements cephalogyres sur la precision dun ajustement visuo-moteur chez l’homme. Journal de Physiologie (Paris), 77, 44A. Roucoux, A. and M. Crommelink, 1980. ‘Eye and head fixation movements: their coordination and control’. In: G.E. Stelmach and J. Requin (eds.), Tutorials in motor behavior. Amsterdam: North-Holland. pp. 305-314. Straschill, M. and F. Schick, 1977. Discharges of superior colliculus neurons during head and eye movements of the alert cat. Experimental Brain Research 27, 131-141. Wurtz. R.M. and J.E. Albano, 1980. Visual motor function of the primate superior colliculus. Annual Review of Neurosciences 3, 189-226.
359
Science 5 (1986) 359-371
HEAD ORIENTING CONTRIBUTES TO THE DIRECTIONAL ACCURACY OF AIMING AT DISTANT TARGETS R. ROLL * Luhoraioire
de Neurosciences
C. BARD LuvcrlUniuersity,
Fonctionelles,
Marseille,
France
Marseille,
France
Quebec, Canada
J. PAILLARD Luboratoire
de Neurosciences
Fonctionelles,
Roll, R., C. Bard and J. Paillard, 1986. Head orienting contributes to the directional accuracy of aiming at distant targets. Human Movement Science 5, 359-371.
The aim of this study was to evaluate the contribution of head orienting to the directional accuracy of aiming at targets of different eccentricities. Six right-handed females were tested in three experimental conditions: (1) aiming at a target with head fixed, (2) aiming with head free to move, (3) aiming with instruction to align head with target. For all conditions, accuracy is reduced when aiming at the more eccentric targets. However, undershooting increases considerably when the head is fixed. The present results support a twofold hypothesis for encoding spatial information of visual origin: an eye ( ~15’ of eccentricity) and a head ( > 25” of eccentricity) range. It can be concluded that head movements contribute to accuracy of aiming at targets located beyond 20’ of eccentricity of the subject’s visual field, thus providing the arm program with directional specifications.
The head, as carrier of the most important captors for distant information, is the leading segment for behavioral activities. Head movements are required for orienting these captors toward sources located in extracorporeal space. In addition, the head contains the labyrinthine apparatus that allows the body to maintain its erect posture with reference to the direction of gravitational force. Changing * Requests for reprints should CNRS, Marseille, France.
0167-9457/87/$3.50
be sent to R. Roll, Laboratoire
0 1987, Elsevier Science Publishers
de Neurosciences
B.V. (North-Holland)
Fonctionelles,
360
R. Roil et al. / Heud orienting,
drrectionul
uccurrrcy, aimrng tusks
postures and movements of the body are organized with reference to head position and head movement. Thus the head, with the combined contribution of visual and vestibular information, is the main agent for the steering of spatially oriented behavior. Steering, however, presupposes a space coordinate system and some invariant or predictable features that allow programmed motor activities to be triggered and guided by visual cues in extracorporeal space. The spatial encoding of visual cues relies heavily on proprioceptive signals of several origins: fovea1 acquisition of the visual target in the retinal coordinate system has to be plotted within the head-centric coordinate system by taking into account both proprioceptive information from extraocular musculature about eye position in the orbit and proprioceptive information of labyrinthine origin about head position in the gravitational field. Finally, the evaluation of body position in relation to head position, that derives from neck proprioceptive information, allows the spatial encoding of the location of a visual target within a body-centric system of coordinates. Hand pointing at a visual target located in the near space of prehension has been extensively studied (reviewed in Paillard and Beaubaton (1978)). If the subject fixates the target, the foveation process is so precise that the directional accuracy of the pointing program of the arm is assumed to depend mainly on the calibration of eye position in the head. Both proprioceptive information from ocular muscle and efferent command of eye movements are presumed to play a role. Provided that vision of arm movement is precluded (the openloop condition excluding corrective feedback of the on-going movement), the accuracy of the pointing movement is taken to reflect the accuracy of the spatial encoding of target position. The coordinated pattern of eye and head movements that is observed when a subject directs his gaze toward a target in an unexpected eccentric position in the visual field is well known. The final gaze orientation has been shown to be independent of neck proprioceptive information provided that the vestibular system is intact (Bizzi 1980). In contrast, the directional accuracy of arm pointing is heavily affected after cervical dorsal root section in monkey (Cohen 1961); and in man, the accuracy of pointing has been shown to be improved when the head is free to move when compared with the head-fixed condition (Roll 1974; Conti 1975; Roll 1976; Marteniuk 1978; Roll et al. 1981; Biguer 1981; Biguer et al. 1984).
R. Roll et al. / Head orientrng,
directionul
accuracy, uimmg tusks
361
Previous studies have shown that the combination of head and eye movements varies with stimulus eccentricity and predictability of target position. Depending on the authors, the eccentricity of the target at which head turning accompanies eye movement varies form 10-15” (Legrand 1952; Crawford 1960) to 35-40” (Mackworth and Mackworth 1958; Bartz 1966). The functional contribution of head orienting to the overall behavioral performance obviously requires clarification (Paillard 1971). This study aims at analyzing the role of head orientation in the localization of a distant target within a body-centric space coordinate system. An aiming task has been used in preference to a classical pointing task for two reasons. (1) Distance coding is thus eliminated as a source of variance in accuracy of the performance. (2) The feedforward programming of the aiming task is presumed to be better tuned than that of a pointing task. In fact, the latter accommodates a rather large margin of inaccuracy within the triggered program of reaching, owing to the remarkable proficiency of visual feedback which assists the on-going movement especially (but not exclusively) during its terminal phase. In contrast, the accuracy of aiming at a distant target is poorly related to corrective feedback of visual origin and therefore relies, even in conditions when vision of the field of action is normal, mainly on the pretuning of the program for positioning the arm in the right orientation. Thus, precluding vision of arm movement should affect aiming less than pointing. Recent studies have shown that aiming and reaching may well rely on two different classes of the preprogramming process that are separately involved in the reorganizational process following prismatic displacement of the visual field (Rip011 1980) and that are selectively affected by pathology according to the locus of the lesion (Brouchon et al. 1980). In order to evaluate the contribution of head orienting to the directional accuracy of aiming, we measured the latter when position of the targets was randomly varied in the visual hemifield ipsilateral to the moving arm and when head constraints were varied. Furthermore, the basic assumption was that each of the body segments concerned - eye, head and trunk - has an optimal working zone at different degrees of eccentricity in the visual field. Accordingly gaze direction can be accurately defined by the calibration of the position of the eye in the orbit within a range of rotation up to 15 O. For gaze direction involving rotation of the eye above 20” of eccentricity, head
362
R. Roll et al. / Heud orienting,
drrectionul
nccuruq.
uiming
task3
rotation would automatically be implicated to bring back the eye within its optimal calibrating range. Then, head-trunk calibration could obey similar boundary constraints at about 40” of eccentricity where a rotation of the shoulder girdle would be required to allow for better calibration of the relative positions of head and trunk. With these considerations in mind, we specified three zones of eccentricity and treated the data accordingly.
Method
Subjects Six right-handed females, aged 25-35, participated as paid subjects. All were tested in three experimental conditions: (1) aiming at the target with head fixed, (2) aiming with head free to move, (3) aiming with instructions to align head with target.
Apparatus The subject was seated with trunk restrained by a seat belt and facing a semi-circular wooden board (180 cm height, 110 cm radius) on which 19 light-emitting diodes (LED) were displayed horizontally at the level of the subject’s eyes. The LEDs were located 9.65 cm apart, subtending a 5” visual angle with respect to the subject’s position. They covered a total visual field of 90”. For biomechanical reasons only targets in the right hemifield were used. In all conditions the subject wore a head-helmet topped by a spot-light designed to project a small luminous arrow on the squared paper covering of the semi-circular panel. Also, she held in her hand another spot-light, identical to the first one but projecting a smaller arrow, with which she points at the target (fig, 1). For each trial the projection on the target of the head and hand spot-lights was photographed with a camera (Olympus 0M2) placed above the subject’s head. In addition, a wooden board was placed horizontally underneath the subject’s chin, to prevent her from viewing either her hand move-
R. Roll ei al. / Head orienting, directionul accumcy, aiming tusks
Fig. 1. Experimental
set-up.
A - frontal
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view; B - top view.
ment or the pointing error on the panel. A chin-rest was mounted on the board for conditions in which the head was restrained. Procedure Subjects were seated in a dimly lit room with both hands resting on their knees, holding a spot-light in their right hand. They were instructed to keep eyes and head facing straight in front of them, thus gazing at the illuminated central diode. Under all experimental conditions and before and after each aiming movement, they had to maintain this resting position and to fixate the central diode until another peripheral target was presented. Then subjects had to direct, as accurately as possible, their spot-light toward the just illuminated target by stretching their arm at full length from the resting position of the hand
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on the knee and to stabilize the spot-light in that direction until the experimenter had made a photograph of the screen and instructed the subject to resume the resting position. No instructions were given concerning the speed of movement execution. Subjects were performing at their spontaneous self-pacing rate (usually in the range of movement time of about 500 msec). They had, however, undergone a training session during which they were allowed to see the projection of their spot-light on the screen and thus to evaluate and correct their aiming error. All subjects performed in three experimental conditions (head constraints): head free to move; head restrained by a chin-rest; and head aligned on target. Each condition involved a total of fifty-four randomly presented trials (9 targets x 6 trials). The targets were located from 5” to 45” of eccentricity, five degrees apart, in the subject’s right hemifield. The picture photographed of each trial against millimetric squared paper on the viewing screen provided a direct and precise recording of head and hand directional errors relative to target position. Differences in size and pattern of the spot-lights on head and arm allow their easy identification on each picture. The results in accuracy of aiming were collapsed within three target zones in accordance with our initial hypothesis: zone 1 included targets of 5”, 10” and 15” of eccentricity; zone 2 included targets of 20”, 25” and 30”, and zone 3 targets of 35”, 40” and 45” of eccentricity. Accuracy was evaluated from three scores: the absolute error, the constant error, and the variable error. Analyses of variance (3 head conditions X 3 zones), with repeated measures on each factor, were applied to each dependent variable.
Results (1) For absolute error, no significant difference was found for the main factors, however, the interaction head/zone was significant F(4, 20) = 2.87, p = -c 0.05, showing an increase of error according to target eccentricity in the head-fixed condition (fig. 2). (2) For constant error, the analysis revealed a significant head condition effect, F(2, 10) = 4.94, p < 0.03; a Duncan post hoc analysis showed that the head-fixed condition significantly differed from the
R. Roll et al. / Head orienting,
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head fixed
3-
I
I
3
1
Z&E
Fig. 2. Absolute
spatial
error according
to head condition
and target zone.
other two conditions (fig. 3). In addition, there was a significant effect of angular zone, F(2, 10) = 13.52, p < 0.01; a Duncan post hoc analysis revealed a significantly larger undershooting in zone 3 than in both other zones. (3) For variable error, no significant difference was found for any of the main factors.
Discussion For all head conditions, accuracy is reduced when aiming at the more eccentric targets. However, undershooting increases considerably when the head is fixed. The hypothesis that man would rely on two modes of encoding spatial information of visual origin provides a possible interpretation of the present results. It seems that up to 15 o of
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head +
position fixed
-+-lined
Fig. 3. Constant
spatial
error according
to head condition
up
and target zone
eccentricity, the arm movement programming is based upon information from the eye-in-head position, mainly computed from saccade amplitude. Prablanc and Biguer (1982) who did not find a significant correlation between hand and eye error, claimed that the efferent copy of the saccade could be used for initiating, rather than computing, the aiming movement. However, as recently suggested by Roll and Roll (1986), the possible influence of proprioceptive extraretinal signal from stretched eye muscles for evaluating the eye-in-head position can not be ruled out, especially as both head and trunk are fixed. The second mode of encoding relies on additional information coming from head position with respect to the trunk and operates beyond 20” of eccentricity, when head movement is systematically associated with eye displacement. Paillard (1976) already suggested that head-position cues would be taken into account in the programming of an arm trajectory at the target, and might contribute to the directional specification within the program of reaching. The head contribution to
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reaching accuracy in slow movements has also been demonstrated by Marteniuk (1978). Thus, a twofold hypothesis for coding is supported by both psychophysiological and neurophysiological data. First, a 15” range is considered as the eye ‘working zone’ (Dodge and Cline 1901; Lancaster 1941). It seems to correspond to a significant value for the oculomotor system, whatever the task to be performed. Bahill et al. (1975) showed that most saccades occurring in natural circumstances reach 15” of eccentricity in man. Second, Biguer et al. (1982; 1984) found a significant difference, beyond 30”, between head-free and head-fixed conditions in an open-loop pointing task. Moreover, the study of temporal organization of head-eye-hand coordination during reaching showed that the neck EMG activity always precedes the eye movement for eccentricities of 20”, 30” and 40”. In the head-fixed condition, the target position is undershot for all angular zones and the error increases as the target eccentricity increases. These results can be considered in relation to neurophysiological data from cat (Blakemore and Donaghy 1980; Roucoux and Crommelink 1980; Straschill and Schick 1977; Harris 1980), and monkey (Wurtz and Albano 1980). These authors indicated two modes of eye-head coordination when stimulating the superior colliculus. With respect to the region of stimulation, small amplitude saccades ( < 20-25”) without head movement, or larger saccades, were observed. If we compare the accuracy of aiming in head-free and head-aligned conditions, it is worth noticing that the most accurate aiming is achieved at 20-30” in the head-centered condition, whereas below this limit the target is overshot; conversely it is undershot beyond 30”. This result brings further evidence to the previous interpretation concerning the eye/head trade-off in the coding of visuo-spatial information according to stimulus eccentricity. Mobilization of the head is not required for small eccentricities (eye range); it leads to an overshoot of the target. The undershooting observed beyond 30” would be the result of shoulder immobilization. Conversely, in the absence of precise instruction concerning head position, namely in the head-free condition, head movements tend to bring the eye back to its working zone, without necessarily centering the head accurately on target. Biguer and Prablanc (1981) claimed that, during gaze orientation toward a visual target, the final head position does not exceed 60% or 70% of target eccentricity. In fact, head movements can be observed, even for small
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Fig. 4. Head-movement
amplitude
of eye and head movers,
according
to target eccentricity.
target eccentricities, according to a typology of individual differences which differentiates between eye and head movers. Such a distinction was introduced by Afanador and Aitsebaomo (1982) in a study of the effects of wearing progressive bifocal spectacles on the normal patterns of eye movement for near visual tasks. They observed that in normal subjects head movements sometimes occur for peripheral stimuli presented as little as two degrees away from the midline. Systematic study on 50 subjects of the range of eye movement before the head moved at least two degrees led to the division of the population into two extreme subgroups: the eye movers who exhibit ranges of eye movement exceeding 20” before moving their head; and the head movers who show ranges of less than 10” before head movement. For example, fig. 4 clearly shows that, for all target eccentricities in the right hemifield, two types of head mobilization can be observed. For eye movers, no head movement is observed up to 15”. From then on, head movement slowly increases in amplitude, and two plateaus are identified: at 25” (head range), and at 35” (shoulder range). Conversely, for head movers, the amplitude of head movement is more important. In fact the head is nearly lined up with the target for all eccentricities. Although these behavioral data might not constitute definitive evidence for the mechanisms involved, they suggest taken in conjunction with the literature on
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the informative role played by neck proprioception, that head movements are part of the aiming program according to target location. Longet (1845) described a ‘cervical ataxia’ syndrome following neck muscle lesions. Cohen’s (1961) results emphasized the role played by the neck proprioceptive receptors over the vestibular contribution in accuracy of movements from a static position. Finally, the existence of a very important pool of neuromuscular receptors in the dorsal neck muscles (Abrahams 1977) suggests a functional role for these receptors in eye/head rotation. Finally experimental support for the influence of cervical proprioception is provided by the chronological analysis of eye/head-hand coordination when a target of more than 15” of eccentricity is presented in the subject’s visual field (Biguer 1981). It was observed that the final head position is reached about 200 msec before the arm final position at the target. This delay could be sufficient to allow a program amendment on the basis of neck proprioceptive feedback, even in an open-loop condition. From the present results, it can be concluded that head movements contribute to the accuracy of aiming at targets located beyond 20” of eccentricity in the subject’s visual field (zone 2). This mechanism should bring the eye back to its optimal working zone. Head position cues could thus be considered in the programming of arm trajectories, specially for directional specifications of eccentric targets. The large undershooting observed in zone 3 may suggest that the accuracy of aiming at target beyond 40” would require the rotation of the shoulder girdle in order to bring the head back within its usual working zone.
References
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