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Proprioceptive information about target location suppresses autokinesis
PROPRIOCEPT~VE INFORMATION ABOUT TARGET LOCATION SUPPRESSES AUTOKINESIS J;LUESR. LACK&~ and Josls J. Z~ZBKAR Brand& University, Waltham, iMr\ 02154, U.S.A. (Received 21 October 1976; in revised form 23 Junrwy
1977)
observers are provided proprioceptive information about the location of a target by allowing them to grasp the target light mount, autokinesis appears after longer latencies, is reduced in magnitude, and is of shorter total duration then when only visual ~~ormation about target location is available. The decrease in autokinetic movement is the consequence of an enhancement of fixation stability when proprioceptive information is available to aid in controlling the direction of regard.
Abstract-When
I,NTRODUCl-ION The autokinetic illusion, the apparent motion of a stationary visuai target, is usually induced by fixating a small target light in an otherwise dark room. Prior to the development of sophisticated navigational guidance systems, autokinesis had practical sign%cance for night flying (Graybiel and Clark, 1945); the illusion remains of concern because of its implications for the perception of visual motion and visual direction. Although autokinesis has been studied systematically since 1896, little agreement exists concerning the factors contributing to its origin; nevertheless, gross loss of fixation stability does appear to be an important factor. The evidence for this claim will be reviewed systematically because it formed the basis for the experiments to be described. These experiments show that subjects can utilize prop~~ep~ve information about limb position to stabilize their direction of gaze and thereby attenuate the magnitude of the autokinetic illusion that they experience. Much of the early work on the relationship between eye movements and the autokinetic illusion was reviewed and experimentally repeated by Skolnick (1940). He specifically called into question the evidence against the involvement of eye movements in autokinesis which had been assembled by Guilford and Dallenbach (1928) in their classic paper on autokinesis. Skolnick pointed out that Guilford and Dallenbach’s photographic measurements of eye position were less sensitive than the eye’s ability to detect the objective movement of a target light against a uniform field. Using improved techniques, Skolnick made photographic records of the eye movements of subjects experiencing autokinesis and established that detectable eye movements were often correlated with reports of autokinesis. In addition, he found that observers viewing magnified comeal reflections from the eyes of subjects experiencing autokinesis could predict with signiIicant accuracy the direction of the autokinetic movements that the subjects reported Skolnick also provided evidence that Exner’s (1896) report of inde~dent apparent motion of a pinhole and a surrounding disc, a report which had been used as evidence against eye movement theories, could be attributed to fading and reappearance of the disc because of adaptation. Using a narrow circle around
the pinhole, instead of a disc, Skolnick found that ~de~dent motion of target and su~ound was vittualiy eliminated. Skolnick failed to confirm Carr’s (1910) claim that, during autokinesis, an afterimage and a target light appear to move together in the same direction-such joint motion would not be expected if eye movements were involved in autokinesis because the image of the target light would be retinally displaced while the afterimage would be ret&tally stable. Nevertheless, Graybiel and Clark (1945) later found support for both Exner’s and Carr’s claims that some components of autokinesis are independent of eye movements. In one experiment, GraybieI and Clark had subjects look through a tube at a red test light with a black cross in its center: subjects reported that the test light would move but was not lost from view and that the cross remained distinct; blurring would have been expected if eye movements greater than severai degrees had displaced the retinal image of the cross beyond the macular area. In a second experiment, subjects reported that a triangular afterimage moved together with a test light, providing confirmation of Carr’s report. These observations led Graybiel and Clark to conclude that eye movements greater in magnitude than 2 or 3” were not essential to the autokinetic illusion. In a more recent experiment, Piggins (1965) reported that when an afterimage and a visual target were viewed simul~eously, most subjects (19 of 15), reported movement of only one tiation object at a time, 15 of the 19 reporting movement of the afterimage only. Three subjects reported conjoint movement of both target objects simultaneously and the remaining three saw simultaneous but not covarying movement of the afterimage and the visual target. Accordingly, Piggins’ observations stress the important contribution of eye movements to autokinesis. While studying the eye movements of steady fixation, Barlow (1952) observed that autokinetic movement occurred only in connection with fixation drifts. This report is of special significance in that Barlow’s eye movement m~surements were more sensitive than those of Guilford and Dallenbach (1928) or Skolnick (1940). Lehman (19651, recording eye movements on an oph~a~o~aph and correfatmg them with reports of stops, starts and changes in the direc-
I.226
JAMES R. LACKYER
ti0R of autokinetic movement, found that reports of autokinetic movement were always preceded within 0.25 set by substantial eye movements and that eye movements were consistently related to stops, starts, and changes in autokinesis. Crone and Verduyn Lunel (19691, measuring what they termed “eccentric fizxation”. found that autokinetic movement was related to drifts of the eye during attempted fixation; they also obtained evidence that eccentricity of fixation k required for the perception of real movement. S~bi~~ation of a target’s retinal image so that lo of horizontal eye movement causes 1’ of retinal image shift has been found by M[atin and MacKinnon (1964) to reduce horizontal autokinesis; nevertheless, although the target image was also partially stabilized in the vertical direction (a 1” vertical eye movement causing a 15’ retinal image shift), vertical autokinesis was greater than in the non-stabilized condition. The latter observation cannot be interpreted in terms of eye movements unless additional assumptions are made. It is known, of course, that autokinesis does not occur with complete stabilization of the retinal image because the target then fades completely within 1-3 set (Yarbus, 1967). Moreover, the miniature eye movements of various forms characteristic of “stable fixation” (Dodge, 1903; Ratcliff and Riggs, 1950; Yarbus, 1967) are not by themselves sufficient to produce autokinesis, or the visual scene would be in constant motion. AIthough an influence of eye movements on autokinesis is apparent., theories about the nature of this influence are quite varied. These theories fall into two general catagories: those proposing that autokinesis results from displacement of the retinal image consequent on invohmtary eye drifts during attempted target fixation, and those suggesting that outflow monitoring of signals for voluntary corrections during fixation is its basis. Hoppe (1894) first proposed the involuntary eye movement theory; more recently, Barlow (1952) and Crone and Verduyn LuneI (1969) have presented substantial experimental support for the role of such large involuntary fixation drifts in autokinesis. By contrast, Whiteside, Graybiel and Niven (1965) have proposed that autokinesis results from the monitoring of efferent signals for re8xation movements. Levy (1972) has proposed a similar model attributing autokinesis to outflow monitoring of the pursuit-like drift corrections that Rashbass (1959) found take piace during attempts at prolonged &ation. A related suggestion by Gregory (1958) and Gregory and Zangwill (1963) attributes autokinesis to a breakdown in the comparison of efferent ~fo~tion about eye position with afferent information about retinal image displacement. The concern here is not to evaiuate which of these various theories provides the best explanation of how eye movements affect autokinesis, but simply to indicate that the experimental evidence ove~he~ngly implicates eye movements as being partially responsible for autokinesis. Levy (1972) has recently reviewed much of the massive literature on the autokinetic phenom~on, and further support for the involvement of eye movements can be obtained in his report. Evidence that oculomotor control can be infiuenced by proprioceptive information about body
and Jo;\?; J. Z~\BK.U
posture wili be briefly discussed to provide background for the experiments to be described. That one can make saccadic eye movements in the dark to fixate the apparent locus of a body part is a well-known fact. The availability of proprioceptive information for the control of pursuit eye movements is less well known. It is generally believed (Robinson, 1968; Alpern, 1972) that retinal image displacement is an essential stimulus for ocular pursuit movements; nevertheless, Lackner and Evanoff (1977) have shown that in complete darkness it is possible to track with continuous eye movements the motion of a tactile stimulus smoothly moving across the body surface. Gregory (195s) has reported that attempts to track one’s moving hand in the dark can elicit smooth pursuit and that an aFterimage projected on to the hand’s apparent position will “lock on” and move smoothly with the hand. Jordan (1970), using objective measurements of eye position. confirmed Gregory’s observations and demonstrated that attempts to track the apparent position of the hand in the dark regularly and reliably evoke pursuit eye movements, when the hand is moved actively or passively over a wide range of veiocities. Lackner (1975) later showed that muscle agerent signals, alone, can reliably evoke pursuit eye movements because subjects, are able to track in complete darkness the illusory motion of their forearm induced by skeletal muscle vibration (cf. Goodwin, McCloskey and Matthews, 1972). Proprioceptive information about hand position is also available for vergence-acco~o~tion control, as can be simply demonstrated by projecting an afterimage on to the apparent locus of the hand in the dark and then slowly moving the hand toward and away from the eyes while attempting to maintain fixation; the afterimage smoothly changes in size, becoming smaller and larger, respectively. Evidence that non-~suai info~tion about body posture can be used to control both version- and vergence-accommodation movements of the eyes, when considered with the substantial evidence that eye movem~ts are important factors in autokinesis. raised the possibility that fixation instability, and consequently autokinesis as well, might be lessened if the observer had stable proprioceptive information about the position of the target light in relation to himself. That is, if stable proprioceptive information about target position can enhance fixation stability, then a reduction should occur in the magnitude and incidence of autokinesis that is experienced. Accordingly, in an initial experiment the latency, duration and magnitude of autokinetic movement were measured under two experimental conditions: (a) while the subject fixated a target light and grasped the base of the target mount; and [b) while the subject merely fixated the target light. It was found that proprioceptive information can be used to reduce significantly the latency, magnitude, and incidence of autokinesir EXPERIMENT
1
Subjects. Ten Brandeis students, e&-it mates and tW0 females, received payment for their voluntary participation. All reported normal vision without glasses Or With Contact lens correction; none were taking drugs or medication.
1227
Suppression of autokinetic movement ,-tpparatus. The fixation target was the tip of a IOmiL fiber optic strand projecting 1 mm from the tapered cud of a cylindrical tube 17.3 cm long and 2.54cm in dia; a remotely controlled pen-light bulb within. the tube could be turned-on to illuminate the fiber optic strand thereby providing a small spot of light During the experiment, the light housing was located btween 36 and 49 cm from the subject’s eyes, placement being determined at the beginning of the experiment according to the subject’s arm length; the housing was secured to the table surface by bolts so that it could not move. The subject’s head was stabiied by a dental acrylic biteboard and movements of the trunk were minimized by seatbelts attached across the chest. An adjustable arm rest was used to support the subject’s arm during those trials in which (s)he was grasping the target light housing. The experiment was conducted in a light-proofed room; the ceiling and walls in the experimental area wete painted flat black to prevent possible reflection of light from the target. Procedure. Each subject participated in two sessions of six trials each. In one session, the subject indicated the onset and duration of autokinesis by depressing a pedal switch connected to a polygraph; in a second session on a later day, the subject indicated the magnitude and direction of autokinetic movement by manipulating a pentipped joy stick that produced a record on graph paper. At the beginning of each session, the subject was settled in position and the target-light stand was placed in the extension of the body’s median plane at a distance that permitted the subject to grasp the housing firmly without arm or shoulder strain. The subject was told that (s)he would be viewing a small light in the otherwise dark room, that (s)he was to futate steadily and to blink as little as possible. In addition, the subject was told that each trial would last 6Osec and during that time the light might appear to move. For the session in which the subject used the foot pedal, (s)he was told to depress the pedal whenever the tight moved, to keep it depressed as Long as the light continued to move, and to release the pedal whenever the light stopped moving. For the session in which the subject used the joy stick, (s)he was told to reproduce the direction and magnitude of target motion with the joy stick and was instructed in its use. After these instructions, the subject was dark-adapted for 5 min; the experiment was then initiated with a practice trial to familiarize the subject with the demands of the task and to make sure that the instructions were understood Fifteen seconds before a trial began, the subject was asked to assume one of two postures: in the look condition (L), the subject’s right hand rested in his/her lap; in the hold condition (H), the subject’s right arm was supported by the arm rest and the subject grasped the light stand firmly, holding his/her thumb near the tip of the light housing. Each session included six trials presented in a balanced
design: five subjects received the order LHHLLH and five received the order HLLHHL. A buzzer beeped with the appearance of the target tight at the beginning of each trial and again when the tar&t light was e~tingu~hed after the &&see trial. Each trial was followed bv a timed 2-min rest period RESULTS
Tables 1 and 2 summarize the observations on of autokinds. Average scores are presented separately for each subject’s L and H conditions because of the considerable inter-subject variability. It can be seen that every subject’s performance is consistent; a longer time elapses in the H condition before the subject reports the onset of autokinesis and the total duration of autokinesis latency and duration
Table 1. Duration of autokinetic movement (in see)
Subject
: 3 4 : 7 8 9 10
While fixating the target tight (L)
While fixating the target light and holding the light stand (H)
7.0 30.3 40.0 11.3 37.3 31.0 9.7 9.3 48.3 23.3
0.0 17.3 25.0 7.7 30.7 25.3 7.7 2.0 34.0 12.7
reported is less than in the L condition. T-tests for correlated samples were performed to compare the H and L conditions: duration scores were significantly different at P < 0.0005 (t = 6.06, one-tailed); latency scores were significantly different at P c 0.005 (t = 4.037, one-tailed). The results of the sessions in which the direction and magnitude of autokinesis was indicated with the joy stick are more difficult to quantify because the traces are not linear nor confined to a general direction. Nevertheless, the maximum distance of excursions from the starting point and the total length of excursion are always less for the H compared to the L conditions. Furthermore, the H conditions often show “oscillation” about a particular region, a fact that supports the subjective impression of several sub jects who reported that autokinetic movements in the H conditions were less excursive than in the L ccinditions, and were frequently of an oscillatory nature. The significant increase in latency and reduction in duration of autokinetic movement for afl subjects in the hold conditions suggests that information about posture can be utilized to improve fixation stability. Reports of several subjects that target light motion during the hold-condition tended to be a small, oscillatory action rather than the more excursive wandering which took place during the look-conditions, suggest that postural information was utilized to reduce the larger drifts associated with fixation instability. Table 2. Latency of autokinetic movement (in set)
Subject 1 2 3 4 5 6 ;I 9 10
While fixating the target light (L)
While furating the target light and holding the light stand (H)
41.6 10.0 8.0 44.0 9.2 12.3 32.0 40.3 3.0 21.5
60.0 17.0 14.0 51.7 13.0 13.0 36.0 42.0 19.3 30.6
I128
J.LWESR.
LACKXER
The report of one subject who experienced double vision of the target light less frequently and with less separation of the images in the hold condition is evidence that postural information about the locus of the target light enhanced the stability of convergence, reducing the phoric movements of the weaker eye. EXPERIMENT
2
To evaluate directly the possibility that proprioceptive information can be utilized to improve fixation stability, measurements of eye posture were made under experimental conditions comparable to those of Experiment 1. Conventional electro-oculography (EOG) was used to monitor horizontal and vertical eye position; such recordings are accurate only to approximately 1” of visual angle; consequently, eye movements of smaller magnitude were below resolution and the results obtained provide information only about how large-amplitude eye movements are affected by the experimental procedures.
and JO,W J.
ZAFIKAR
COKcLCSION
It has been demonstrated that- some of the involuntary eye movements associated with prolonged steady fixation can be attenuated if the subject has proprioceptive information about target location. In conjunction with the demonstrations that pursuit eye movements can be evoked in total darkness by propriocep tive signals (Gregory, 1958; Jordan, 1970X by muscle afferent signals (Lackner, 1973, and by tactile signals (Lackner and Evanoff, 1977), the present observations emphasize the availability of spatial information about posture in the control of steady-state eye position as well as in the control of pursuit and saccadic eye movements. Acknowledgements-Tbis research was supported in part bv the Swncer Foundation. the Rosenstiel Biomedical Sciences goundation and NASA Grant NGL-22-009-308. J.R.L. is also at the Department of Psychology, Massachusetts Institute of Technology, Cambridge, MA 02139, U.S.A.
Method Subjects.
Nine Brandeis undergraduates were recruited for their voluntary, paid participation. All had normal visual acuity without glasses or with contact lens correction. Procedure. The instructions to the subjects and the procedure followed were identical to the sessions in Experiment 1 in which the onset and duration of autokinesis were indicated by depressing a foot pedal. In addition, the horizontal positions of the subject’s eyes were monitored by means of EGG recordings and displayed on separate channels of a Grass model 7 polygraph. During the experimental trials, depression of the foot pedal by the subject [signalling that (s)he was experiencing autokinesis], produced a pen deflection on another of the polygraph channels thereby permitting a correlation of eye movement patterns with reports of autokinesis. RESULTS
All subjects reported autokinesis more often in the L condition. The eye movement recordings were analyzed for evidence of eye deviation during the period 500 msec prior to each report of autokinesis. For the H condition, 28 of 79 reports of autokinesis were preceded by eye movements of sufficient magnitude to be visible on the EOG records. By contrast, in the L condition, 98 of 140 reports of autokinesis were associated with eye movements greater than I” in amplitude. DlSCUSSlOFi Despite the limitation in recording sensitivity, which only allowed eye movements greater than 1” to be detected with absolute reliability, the results indicate an improvement in fixation stability when proprioceptive information about target location is avail-
able to assist oculomotor control during prolonged attempts at fixation. Both the incidence and the magnitude of large involuntary eye drifts during attempted fixation are reduced by the presence of proprioceptive cues indicating target position. This enhancement of fixation stability is reflected in an increase in the latent period before autokinesis is first experienced and in a reduction of the magnitude and duration
of autokinetic
movement
experienced.
REFEREUCES
Alpern M. (1972) Eye movements. In Handbook of Sensory Phvsiolouv (Edited bv Jameson D. and Hurvich L.). I. Vol. Vii/4, ~6: jO3-330. Springer. Berlin. Barlow H. B. (1952) Eye movements during fixation. J. Physiol., Lond. 116, 290-306. Carr H. A. (1910) The autokinetic sensation. Psvchol. Rea 17, 42-7j: ’ Crone R. A. and Verdeyn Lunel H. F. E. (1969) Autokinesis and the perception of movement: the physiology of eccentric fixation. Vision Res. 9, 89-101. 0odge R. (1903) Five types of eye movement. Am J. Physiol. 8, 307-329.
Exner S. (1896) Uber autokinetiche Emp6ndungen. Z. Psychol. Physiol. Sinnesorg. 12, 313-330. Goodwin G. M., McCloskey D. I. and Matthews P. B. C. (1972) The contribution of muscle afferents to kinesthesia shown by vibration induced illusions of movement and by the effects of paralyzing joint afferents. Brain 95, 705-748. Graybiel A. and Clark B. (1945) Autokinetic illusion and itb significance in night f&ing.’ Nav. Sch. of Aviat. Med USN Air Tmg Bases. Pensacola\ Florida. Rep, . No. 3 II-IV, 146. Gregory R. L. (1958) Eye movements and the stability of the visual world. Nature, Lmd. 182, 1214-1216. Gregory R. L. and ZangwilI 0. L. (1963) The origin of the autokinetic effect. Q. J. exp. Psychol. 15, 252-261. Guilford J. P. and Dalleibach k. M: (1928) A study of the autokinetic sensation. Am. J. Psvchol. 40, 83-91. Hopue J. (1894) Studie zur Erklarung g*&visser!%heinbeweg;gen.‘ Z. Psychol. Physiol. .Sinn&rg. 7, 29-37. Jordan S. (19701 Ocular oursuit movement as a function of visual‘and &oprioce$ive stimulation. Vision Res. 10, 775-780.
Lackner J. R. (1975) Pursuit eye movements elicited by muscle afferent information. Neurosci. Len. 1, 25-28. Lackner J. R. and Evanoff J. E. (1977) Smooth pursuit eye movements elicited by somatosensory stimulation. Neurosci. Lett. 4. 43-48. Lehman R. S. (1965) Eye-movements and the autokinetic illusion. Am J. Psvchol. 78, 490-492 Levy J. (1972) Autoknetic ill&ion: a systematic review of theories, measures, and independent variables. Psychol. Bull. 78, 457-474.
Matin L. and MacKinnon G. E. (1964) Autokinetic movement: selective manipulation of directional components bv > image I stabilization. Science 143, 147-148.
Suppression of autokinetic movement Pig-&s D. J. (1965) Autokinesis with an afterimage. Am J. Psychol.
18. 509-510.
Rashbass C. (1959) Barbituate nystagmus and the mechanisms of visual fixation. Xature. Land. 183, 597. Ratliff F. and Riggs L. A. (1950) Involuntary motions of the eye during monocular fixation. J. e.xp. Psycho!. 40. 657-7OL.
Robinson D. A. (1968) The oculomotor control system: a review. Proc. Insm elect. Engrs 56, 1032-1047.
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Skolnick A. (1940) The role of eye movements in the autokinetic phenomenon. J. exp. Psychol. 16. 373-393. Whiteside T. C. D., Graybiel A. and Niven J. I. (1965) Visual illusions of movement. Brain 88. 193-210. Yarbus A. L. (1967) Epe tnocemenrs cutd Vision. Plenum Press. New York.
1977)
observers are provided proprioceptive information about the location of a target by allowing them to grasp the target light mount, autokinesis appears after longer latencies, is reduced in magnitude, and is of shorter total duration then when only visual ~~ormation about target location is available. The decrease in autokinetic movement is the consequence of an enhancement of fixation stability when proprioceptive information is available to aid in controlling the direction of regard.
Abstract-When
I,NTRODUCl-ION The autokinetic illusion, the apparent motion of a stationary visuai target, is usually induced by fixating a small target light in an otherwise dark room. Prior to the development of sophisticated navigational guidance systems, autokinesis had practical sign%cance for night flying (Graybiel and Clark, 1945); the illusion remains of concern because of its implications for the perception of visual motion and visual direction. Although autokinesis has been studied systematically since 1896, little agreement exists concerning the factors contributing to its origin; nevertheless, gross loss of fixation stability does appear to be an important factor. The evidence for this claim will be reviewed systematically because it formed the basis for the experiments to be described. These experiments show that subjects can utilize prop~~ep~ve information about limb position to stabilize their direction of gaze and thereby attenuate the magnitude of the autokinetic illusion that they experience. Much of the early work on the relationship between eye movements and the autokinetic illusion was reviewed and experimentally repeated by Skolnick (1940). He specifically called into question the evidence against the involvement of eye movements in autokinesis which had been assembled by Guilford and Dallenbach (1928) in their classic paper on autokinesis. Skolnick pointed out that Guilford and Dallenbach’s photographic measurements of eye position were less sensitive than the eye’s ability to detect the objective movement of a target light against a uniform field. Using improved techniques, Skolnick made photographic records of the eye movements of subjects experiencing autokinesis and established that detectable eye movements were often correlated with reports of autokinesis. In addition, he found that observers viewing magnified comeal reflections from the eyes of subjects experiencing autokinesis could predict with signiIicant accuracy the direction of the autokinetic movements that the subjects reported Skolnick also provided evidence that Exner’s (1896) report of inde~dent apparent motion of a pinhole and a surrounding disc, a report which had been used as evidence against eye movement theories, could be attributed to fading and reappearance of the disc because of adaptation. Using a narrow circle around
the pinhole, instead of a disc, Skolnick found that ~de~dent motion of target and su~ound was vittualiy eliminated. Skolnick failed to confirm Carr’s (1910) claim that, during autokinesis, an afterimage and a target light appear to move together in the same direction-such joint motion would not be expected if eye movements were involved in autokinesis because the image of the target light would be retinally displaced while the afterimage would be ret&tally stable. Nevertheless, Graybiel and Clark (1945) later found support for both Exner’s and Carr’s claims that some components of autokinesis are independent of eye movements. In one experiment, GraybieI and Clark had subjects look through a tube at a red test light with a black cross in its center: subjects reported that the test light would move but was not lost from view and that the cross remained distinct; blurring would have been expected if eye movements greater than severai degrees had displaced the retinal image of the cross beyond the macular area. In a second experiment, subjects reported that a triangular afterimage moved together with a test light, providing confirmation of Carr’s report. These observations led Graybiel and Clark to conclude that eye movements greater in magnitude than 2 or 3” were not essential to the autokinetic illusion. In a more recent experiment, Piggins (1965) reported that when an afterimage and a visual target were viewed simul~eously, most subjects (19 of 15), reported movement of only one tiation object at a time, 15 of the 19 reporting movement of the afterimage only. Three subjects reported conjoint movement of both target objects simultaneously and the remaining three saw simultaneous but not covarying movement of the afterimage and the visual target. Accordingly, Piggins’ observations stress the important contribution of eye movements to autokinesis. While studying the eye movements of steady fixation, Barlow (1952) observed that autokinetic movement occurred only in connection with fixation drifts. This report is of special significance in that Barlow’s eye movement m~surements were more sensitive than those of Guilford and Dallenbach (1928) or Skolnick (1940). Lehman (19651, recording eye movements on an oph~a~o~aph and correfatmg them with reports of stops, starts and changes in the direc-
I.226
JAMES R. LACKYER
ti0R of autokinetic movement, found that reports of autokinetic movement were always preceded within 0.25 set by substantial eye movements and that eye movements were consistently related to stops, starts, and changes in autokinesis. Crone and Verduyn Lunel (19691, measuring what they termed “eccentric fizxation”. found that autokinetic movement was related to drifts of the eye during attempted fixation; they also obtained evidence that eccentricity of fixation k required for the perception of real movement. S~bi~~ation of a target’s retinal image so that lo of horizontal eye movement causes 1’ of retinal image shift has been found by M[atin and MacKinnon (1964) to reduce horizontal autokinesis; nevertheless, although the target image was also partially stabilized in the vertical direction (a 1” vertical eye movement causing a 15’ retinal image shift), vertical autokinesis was greater than in the non-stabilized condition. The latter observation cannot be interpreted in terms of eye movements unless additional assumptions are made. It is known, of course, that autokinesis does not occur with complete stabilization of the retinal image because the target then fades completely within 1-3 set (Yarbus, 1967). Moreover, the miniature eye movements of various forms characteristic of “stable fixation” (Dodge, 1903; Ratcliff and Riggs, 1950; Yarbus, 1967) are not by themselves sufficient to produce autokinesis, or the visual scene would be in constant motion. AIthough an influence of eye movements on autokinesis is apparent., theories about the nature of this influence are quite varied. These theories fall into two general catagories: those proposing that autokinesis results from displacement of the retinal image consequent on invohmtary eye drifts during attempted target fixation, and those suggesting that outflow monitoring of signals for voluntary corrections during fixation is its basis. Hoppe (1894) first proposed the involuntary eye movement theory; more recently, Barlow (1952) and Crone and Verduyn LuneI (1969) have presented substantial experimental support for the role of such large involuntary fixation drifts in autokinesis. By contrast, Whiteside, Graybiel and Niven (1965) have proposed that autokinesis results from the monitoring of efferent signals for re8xation movements. Levy (1972) has proposed a similar model attributing autokinesis to outflow monitoring of the pursuit-like drift corrections that Rashbass (1959) found take piace during attempts at prolonged &ation. A related suggestion by Gregory (1958) and Gregory and Zangwill (1963) attributes autokinesis to a breakdown in the comparison of efferent ~fo~tion about eye position with afferent information about retinal image displacement. The concern here is not to evaiuate which of these various theories provides the best explanation of how eye movements affect autokinesis, but simply to indicate that the experimental evidence ove~he~ngly implicates eye movements as being partially responsible for autokinesis. Levy (1972) has recently reviewed much of the massive literature on the autokinetic phenom~on, and further support for the involvement of eye movements can be obtained in his report. Evidence that oculomotor control can be infiuenced by proprioceptive information about body
and Jo;\?; J. Z~\BK.U
posture wili be briefly discussed to provide background for the experiments to be described. That one can make saccadic eye movements in the dark to fixate the apparent locus of a body part is a well-known fact. The availability of proprioceptive information for the control of pursuit eye movements is less well known. It is generally believed (Robinson, 1968; Alpern, 1972) that retinal image displacement is an essential stimulus for ocular pursuit movements; nevertheless, Lackner and Evanoff (1977) have shown that in complete darkness it is possible to track with continuous eye movements the motion of a tactile stimulus smoothly moving across the body surface. Gregory (195s) has reported that attempts to track one’s moving hand in the dark can elicit smooth pursuit and that an aFterimage projected on to the hand’s apparent position will “lock on” and move smoothly with the hand. Jordan (1970), using objective measurements of eye position. confirmed Gregory’s observations and demonstrated that attempts to track the apparent position of the hand in the dark regularly and reliably evoke pursuit eye movements, when the hand is moved actively or passively over a wide range of veiocities. Lackner (1975) later showed that muscle agerent signals, alone, can reliably evoke pursuit eye movements because subjects, are able to track in complete darkness the illusory motion of their forearm induced by skeletal muscle vibration (cf. Goodwin, McCloskey and Matthews, 1972). Proprioceptive information about hand position is also available for vergence-acco~o~tion control, as can be simply demonstrated by projecting an afterimage on to the apparent locus of the hand in the dark and then slowly moving the hand toward and away from the eyes while attempting to maintain fixation; the afterimage smoothly changes in size, becoming smaller and larger, respectively. Evidence that non-~suai info~tion about body posture can be used to control both version- and vergence-accommodation movements of the eyes, when considered with the substantial evidence that eye movem~ts are important factors in autokinesis. raised the possibility that fixation instability, and consequently autokinesis as well, might be lessened if the observer had stable proprioceptive information about the position of the target light in relation to himself. That is, if stable proprioceptive information about target position can enhance fixation stability, then a reduction should occur in the magnitude and incidence of autokinesis that is experienced. Accordingly, in an initial experiment the latency, duration and magnitude of autokinetic movement were measured under two experimental conditions: (a) while the subject fixated a target light and grasped the base of the target mount; and [b) while the subject merely fixated the target light. It was found that proprioceptive information can be used to reduce significantly the latency, magnitude, and incidence of autokinesir EXPERIMENT
1
Subjects. Ten Brandeis students, e&-it mates and tW0 females, received payment for their voluntary participation. All reported normal vision without glasses Or With Contact lens correction; none were taking drugs or medication.
1227
Suppression of autokinetic movement ,-tpparatus. The fixation target was the tip of a IOmiL fiber optic strand projecting 1 mm from the tapered cud of a cylindrical tube 17.3 cm long and 2.54cm in dia; a remotely controlled pen-light bulb within. the tube could be turned-on to illuminate the fiber optic strand thereby providing a small spot of light During the experiment, the light housing was located btween 36 and 49 cm from the subject’s eyes, placement being determined at the beginning of the experiment according to the subject’s arm length; the housing was secured to the table surface by bolts so that it could not move. The subject’s head was stabiied by a dental acrylic biteboard and movements of the trunk were minimized by seatbelts attached across the chest. An adjustable arm rest was used to support the subject’s arm during those trials in which (s)he was grasping the target light housing. The experiment was conducted in a light-proofed room; the ceiling and walls in the experimental area wete painted flat black to prevent possible reflection of light from the target. Procedure. Each subject participated in two sessions of six trials each. In one session, the subject indicated the onset and duration of autokinesis by depressing a pedal switch connected to a polygraph; in a second session on a later day, the subject indicated the magnitude and direction of autokinetic movement by manipulating a pentipped joy stick that produced a record on graph paper. At the beginning of each session, the subject was settled in position and the target-light stand was placed in the extension of the body’s median plane at a distance that permitted the subject to grasp the housing firmly without arm or shoulder strain. The subject was told that (s)he would be viewing a small light in the otherwise dark room, that (s)he was to futate steadily and to blink as little as possible. In addition, the subject was told that each trial would last 6Osec and during that time the light might appear to move. For the session in which the subject used the foot pedal, (s)he was told to depress the pedal whenever the tight moved, to keep it depressed as Long as the light continued to move, and to release the pedal whenever the light stopped moving. For the session in which the subject used the joy stick, (s)he was told to reproduce the direction and magnitude of target motion with the joy stick and was instructed in its use. After these instructions, the subject was dark-adapted for 5 min; the experiment was then initiated with a practice trial to familiarize the subject with the demands of the task and to make sure that the instructions were understood Fifteen seconds before a trial began, the subject was asked to assume one of two postures: in the look condition (L), the subject’s right hand rested in his/her lap; in the hold condition (H), the subject’s right arm was supported by the arm rest and the subject grasped the light stand firmly, holding his/her thumb near the tip of the light housing. Each session included six trials presented in a balanced
design: five subjects received the order LHHLLH and five received the order HLLHHL. A buzzer beeped with the appearance of the target tight at the beginning of each trial and again when the tar&t light was e~tingu~hed after the &&see trial. Each trial was followed bv a timed 2-min rest period RESULTS
Tables 1 and 2 summarize the observations on of autokinds. Average scores are presented separately for each subject’s L and H conditions because of the considerable inter-subject variability. It can be seen that every subject’s performance is consistent; a longer time elapses in the H condition before the subject reports the onset of autokinesis and the total duration of autokinesis latency and duration
Table 1. Duration of autokinetic movement (in see)
Subject
: 3 4 : 7 8 9 10
While fixating the target tight (L)
While fixating the target light and holding the light stand (H)
7.0 30.3 40.0 11.3 37.3 31.0 9.7 9.3 48.3 23.3
0.0 17.3 25.0 7.7 30.7 25.3 7.7 2.0 34.0 12.7
reported is less than in the L condition. T-tests for correlated samples were performed to compare the H and L conditions: duration scores were significantly different at P < 0.0005 (t = 6.06, one-tailed); latency scores were significantly different at P c 0.005 (t = 4.037, one-tailed). The results of the sessions in which the direction and magnitude of autokinesis was indicated with the joy stick are more difficult to quantify because the traces are not linear nor confined to a general direction. Nevertheless, the maximum distance of excursions from the starting point and the total length of excursion are always less for the H compared to the L conditions. Furthermore, the H conditions often show “oscillation” about a particular region, a fact that supports the subjective impression of several sub jects who reported that autokinetic movements in the H conditions were less excursive than in the L ccinditions, and were frequently of an oscillatory nature. The significant increase in latency and reduction in duration of autokinetic movement for afl subjects in the hold conditions suggests that information about posture can be utilized to improve fixation stability. Reports of several subjects that target light motion during the hold-condition tended to be a small, oscillatory action rather than the more excursive wandering which took place during the look-conditions, suggest that postural information was utilized to reduce the larger drifts associated with fixation instability. Table 2. Latency of autokinetic movement (in set)
Subject 1 2 3 4 5 6 ;I 9 10
While fixating the target light (L)
While furating the target light and holding the light stand (H)
41.6 10.0 8.0 44.0 9.2 12.3 32.0 40.3 3.0 21.5
60.0 17.0 14.0 51.7 13.0 13.0 36.0 42.0 19.3 30.6
I128
J.LWESR.
LACKXER
The report of one subject who experienced double vision of the target light less frequently and with less separation of the images in the hold condition is evidence that postural information about the locus of the target light enhanced the stability of convergence, reducing the phoric movements of the weaker eye. EXPERIMENT
2
To evaluate directly the possibility that proprioceptive information can be utilized to improve fixation stability, measurements of eye posture were made under experimental conditions comparable to those of Experiment 1. Conventional electro-oculography (EOG) was used to monitor horizontal and vertical eye position; such recordings are accurate only to approximately 1” of visual angle; consequently, eye movements of smaller magnitude were below resolution and the results obtained provide information only about how large-amplitude eye movements are affected by the experimental procedures.
and JO,W J.
ZAFIKAR
COKcLCSION
It has been demonstrated that- some of the involuntary eye movements associated with prolonged steady fixation can be attenuated if the subject has proprioceptive information about target location. In conjunction with the demonstrations that pursuit eye movements can be evoked in total darkness by propriocep tive signals (Gregory, 1958; Jordan, 1970X by muscle afferent signals (Lackner, 1973, and by tactile signals (Lackner and Evanoff, 1977), the present observations emphasize the availability of spatial information about posture in the control of steady-state eye position as well as in the control of pursuit and saccadic eye movements. Acknowledgements-Tbis research was supported in part bv the Swncer Foundation. the Rosenstiel Biomedical Sciences goundation and NASA Grant NGL-22-009-308. J.R.L. is also at the Department of Psychology, Massachusetts Institute of Technology, Cambridge, MA 02139, U.S.A.
Method Subjects.
Nine Brandeis undergraduates were recruited for their voluntary, paid participation. All had normal visual acuity without glasses or with contact lens correction. Procedure. The instructions to the subjects and the procedure followed were identical to the sessions in Experiment 1 in which the onset and duration of autokinesis were indicated by depressing a foot pedal. In addition, the horizontal positions of the subject’s eyes were monitored by means of EGG recordings and displayed on separate channels of a Grass model 7 polygraph. During the experimental trials, depression of the foot pedal by the subject [signalling that (s)he was experiencing autokinesis], produced a pen deflection on another of the polygraph channels thereby permitting a correlation of eye movement patterns with reports of autokinesis. RESULTS
All subjects reported autokinesis more often in the L condition. The eye movement recordings were analyzed for evidence of eye deviation during the period 500 msec prior to each report of autokinesis. For the H condition, 28 of 79 reports of autokinesis were preceded by eye movements of sufficient magnitude to be visible on the EOG records. By contrast, in the L condition, 98 of 140 reports of autokinesis were associated with eye movements greater than I” in amplitude. DlSCUSSlOFi Despite the limitation in recording sensitivity, which only allowed eye movements greater than 1” to be detected with absolute reliability, the results indicate an improvement in fixation stability when proprioceptive information about target location is avail-
able to assist oculomotor control during prolonged attempts at fixation. Both the incidence and the magnitude of large involuntary eye drifts during attempted fixation are reduced by the presence of proprioceptive cues indicating target position. This enhancement of fixation stability is reflected in an increase in the latent period before autokinesis is first experienced and in a reduction of the magnitude and duration
of autokinetic
movement
experienced.
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