- Email: [email protected]
Oculomotor tonus and visual adaptation
Acta Psychologica 63 (1986) 213-231 North-Holland
OCULQMOTOR
TONUS AND VISUAL
213
ADAPTATION
*
D. Alfred OWENS Franklin & Marshall College, Lmzcaster, USA Accepted March 1986
The contribution of oculomotor efference to visual perception and performance can be clarified by considering the functions of tonus. Accommodation and vergence typically ‘relax’ at an intermediate distance, reflecting tonic innervation of the ciliary and extraocular muscles, which varies widely among individuals who have normal vision. In many situations, especially when stimulation is degraded, fixation and focusing responses are biased toward the individual’s resting state. Moreover, unusual circumstances, such as alteration of the relation of eye position and distanceor prolonged exposure to near work, induce adaptive modification of the resting posture. Thesenormal variations of oculomotor tonus affect the accuracy and the effort required to fixate objects,and they may help explain problems of space perception and visual fatigue.
1. Introduction This paper examines the role of oculomotor tonus in two phenomena that have a long history in the study of vision. The first, which is somewhat closer to the issue of perceiving three-dimensional space, concernsthe manner in which accommodation and vergence eye movements affect distance perception. The second, which is more closely related to acting in three-dimensional space, concerns the contribution of oculomotor processes to symptoms of visual fatigue. Following traditional theories (Helmholtz 1867; Maddox 1893), previous inquiries into both of these problems have assumed that accommodation and * This paper is based on a presentation at the Conference on Sensorimotor Interactions in Space Perception and Action at the Zentrum fir interdisziplinlre Forschung (ZiF) der UniversitPt Bielefeld in February, 1985. I want to thank Annie Vinter for helping to translate Descartes. Preparation of this paper was supported by ZiF and Franklin & Marshall College; the research wassupported in part by Grant EY-03898 from the National Eye Institute. Mailing address: D.A. Owens, Whitely Psychology Laboratories, Franklin & Marshall College, P.O.Box 3003, Lancaster, PA 17604-3003, USA. OoOl-6918/86/$3.50 0 1986, Elsevier Science Publishers B.V. (North-Holland)
214
D.A. Owens / Oculomotor tonus und visual adapotion
vergence adjust to optical infinity at rest. We now know this is not the case (Owens 1984). Rather, both systems adopt intermediate postures at rest. Abandoning the old view requires a new conception of the processes controlling accommodation and vergence and of their functional impact on perception and performance. It introduces a new approach to perceptual problems that arise under low visibility conditions, and it suggests a new interpretation of the adaptive changes found with exposure to effortful visual tasks and with alterations of the relation of eye position and environmental space.
2. Accommodation, vergence, and distance perception One of the oldest hypotheses in the literature on vision is that eye position, particularly binocular vergence, provides information about the location of objects in space. Descartes (1664) argued that we have the innate capacity to sense the angle of convergence and ‘compute’, by some sort of unconscious geometry, the distance of fixated objects. He was also the first to describe accurately the mechanism of visual accommodation and to propose that accommodative, as well as vergence, responses contribute to distance perception (fig. 1). Although Descartes’ theory did not survive intact, the notion that distance perception depends at least partly on vergence and accommodation did. Berkeley (1709) argued that, while it is absurd to explain distance perception in terms of innate geometric ideas that are quite inaccessible to conscious awareness, it is reasonable to assume that we acquire oculomotor information about distance through the association of eye-muscle sensations with distance sensations provided by tactual interactions with the environment. His work may be the clearest early statement of the theory that we must learn to perceive three-dimensional space and that ‘the hand educates the eye’. These ideas were inherited by experimental psychology and soon began to lose credibility. The experimental evidence collected by Wundt (1862), Helmholtz (1867), Baird (1903) and many others showed that people do not perceive depth and distance as accurately as the philosophers had supposed, at least not under laboratory conditions designed to isolate oculomotor information. While the results and interpretations varied, the evidence was fairly consistent on two points: (1) binocular judgements are more accurate than monocular observations, although
Fis. lb.
Fig. 1. Descartes’ (1664) sketches of oculomotor mechanisms of distance perception. Fig. 11 illustrates his accurate model of visual accommodation: the crystalline lens must assume shapes ‘I’ and ‘F’ to focus distances ‘X’ and ‘T’, respectively. Vergence angle and distance (fig. 16) were thought to be perceived by innate geometry, just as the blind man (fig. 15) perceives the angles and distance of the intersecting sticks. Reprinted from Descartes, R., 1664. ‘Le monde. Trait& de l’homme’. In: C. Adam and P. Tannery (eds.), Oeuvres de Descartes, Vol. XI, Paris: Librairie Philosophie J. Vrin, 1967. pp. 155-162.
Pip. IS.
c: VI
216
D.A. Owens / Oculomotor tonus and visual aduptation
neither are very accurate; (2) subjects vary widely in their errors, with some tending to underestimate distance (e.g., Wundt 1862), and others tending to overestimate distance (e.g., Hehnholtz 1867). The poor accuracy and high variability of such data contributed to the view that oculomotor information is less effective than ‘pictorial cues’ for distance. A common finding of studies of space perception under ‘reduced cue’ conditions, is that judgements of size and distance tend to be biased toward a distance of 1 or 2 meters (Swenson 1932; Foley 1980). This perceptual bias was studied most extensively by Gogel (1969, 1977) who referred to the phenomenon as the ‘specific distance tendency’ (SIP). According to Gogel, the SDT represents an ‘autochthonic’ perceptual bias that operates in combination with pictorial and oculomotor cues to determine perceived distance. The influence of the SDT increases as other information decreases. Therefore, it is best measured in conditions devoid of distance information, as with a small luminous target viewed monocularly in darkness. Such measures show considerable intersubject variability, with SDT values ranging from about 30 cm to several meters. The SDT was an appealing concept because it explained a variety of spatial illusions in terms of a common process, a systematic bias of perceived distance under reduced stimulus conditions. At the same time, this concept raised new questions about why perception is biased toward an intermediate distance, ,and why this bias exhibits such wide individual differences. New research on accommodation provided a clue to the possible basis of the SDT. The development of the laser-Badal optometer (Hennessy and Leibowitz 1972) allowed measurement of ocular refraction without stimulating accommodation, enabling us to reexamine an old controversy about the resting state of accommodation. As noted earlier, popular theories claimed that the eyes relax at the far point of their operating range. Accordingly, oculomotor effort was thought to be necessary only to see near stimuli, while passive forces (such as elasticity of supporting tissues) were thought to shift focus and fixation from near to distant stimuli. This view was not unanimous, however. Over the past 130 years it has been challenged by several authors, who proposed instead that accommodation relaxes at an intermediate distance (Weber 1855, .cited by Cornelius 1861; Cogan 1937; Morgan 1946; Schober 1954). The intermediate resting state hypothesis was appealing because (1) it implied that accommodation, like most other
D.A. Owens / Oculomotor tonus and visual adaptation
217
motor systems, is comprised of opponent (near and far) mechanisms, and (2) it offered a simple explanation for ‘anomalous myopias’ that appear under reduced stimulus conditions and seem paradoxical from the traditional viewpoint (Leibowitz and Owens 1978). There were few data to support this novel hypothesis, however, and it had little impact on mainstream theory and practice. Early studies with the laser optometer provided new evidence for the intermediate resting state hypothesis. Measurements of the ‘dark focus’ showed that most subjects accommodate to an intermediate distance in darkness. They also revealed unexpectedly wide variability among subjects with normal vision. One large sample yielded individual dark focus values ranging from infinity to 4 diopters (D; 25 cm), with an average of 1.5 D, or 67 cm (fig. 2A). Furthermore, measures taken under a wide variety of conditions showed that focusing responses for visible targets are often biased toward the subject’s dark focus, especially under degraded stimulus conditions (Leibowitz and Owens 1978). So the laser optometer not only revived the intermediate resting state hypothesis, but also provided a new insight regarding normal variations of the behavior of accommodation. The operating range of accommodation depends on the strength of available stimulation (fig. 2B). Whenever stimulation is reduced, subjects generally become increasingly myopic for distant stimuli and hyperopic for near stimuli. These normal variations of accommodation suggested an alternative explanation for the SDT. Conditions used to measure the SDT provided little or no feedback for accommodation. Therefore, subjects would most likely focus for an intermediate distance, and this bias might influence distance perception. A comparison of the dark focus and the SDT showed no relationship, however. Although both the average dark focus and SDT values corresponded to intermediate distances (41 and 145 cm, respectively) the measures of individual subjects were not significantly correlated (fig. 3A). While this finding ruled out the hypothesis that the SDT results from errors of accommodation, it did not eliminate the possible involvement of binocular vergence. This possibility seemed unlikely at first because vergence and accommodation are normally closely correlated (Morgan 1968). We therefore assumed they would adjust to the same distance at rest. As with accommodation, traditional theories of vergence held that the eyes return to a parallel or slightly divergent position at rest (Maddox 1893). But later work showed that vergence
D.A. Owens / Oculomotor tonus and visual adaptation
218
30
N=220 Mean = 1.52 SD. = 0.77
25 20
r
15 10 5
33
25
cm
FCCUS IN DARKNESS 5 -B 2 al --5
Strong
4 =
Stimulation
I $ ti “,i Lrl a
D E
Weaker
:
2.
3-
i
: a ‘; 2 xl
1 -
No Stimulation
5
0
0 M
I 100
2 50
STIMULUS (cm and diopters
3 33
4 25
Stimulation
5
D-MA
20
cm
DISTANCE
or meter-angles.
D-MA)
Fig. 2. (A) Distribution of dark focus values of 220 college students. Contrary to classical theory, the resting focus corresponds to an intermediate distance and shows wide intersubject variability. (B) As stimulation is degraded, accommodation and vergence responses are progressively biased toward the observer’s resting posture. This bias typically results in increasing ‘myopic’ or ‘esophotic’ errors for distant targets and increasing ‘hyperopic’ or ‘exophoric’ errors for near targets. Fig. 2A reprinted from Leibowitz, H.W. and D.A. Owens, 1978. New evidence for the intermediate position of relaxed accommodation. Documenta Ophthalmologica 46, p. 136; fig. 2B reprinted from Owens, D.A., in press. ‘Oculomotor information and perception of three-dimensional space’. In: H. Heuer and A.F. Sanders (eds.), Perspectives on perception and action. Hillsdale, NJ: Erlbaum.
D.A. Owens / Oculomotor tonus und visual adaptation
m
219
220
D.A. Owens / Oculomotor tows and visuul adaptation
also shifts toward an intermediate posture when illumination is reduced (Ivanoff and Bourdy 1954). Moreover, one study had reported that vergence and accommodation dissociate ‘in the absence of retinal images’ (Fincham 1962). This suggested that they might rest at different distances. If so, then the SDT might be related to vergence rather than to accommodation. We tested this hypothesis in a second experiment which compared subjects’ SDT with their ‘dark vergence’ posture (Owens and Leibowitz 1976). This time the data showed a significant correlation (fig. 3B). So it appeared that, although the dark focus has little or no effect on space perception, dark vergence posture is related to distance perception in low illumination. This correlation does not necessarily mean that the SDT is caused by dark vergence, but it does suggest that spatial illusions encountered under degraded visual conditions are related to vergence behavior. This interpretation was reinforced by two subsequent studies. In an investigation of vergence for dim peripheral stimuli, Ellie Francis and I (1983) found that, as stimulus eccentricity increases, responses are increasingly biased toward the observer’s dark vergence posture. Thus, like the dark focus bias, vergence responses are progressively biased toward the resting position as disparity information is degraded (fig. 2B). In another study, Post and Leibowitz (1982) found that ‘illusory concomitant motion’, which can occur with head movements in low illumination, results from an anomalous interaction between voluntary pursuit and reflexive eye movement systems. They traced this phenomenon to inappropriate ‘gain’ of the vestibulo-ocular reflex, which results from the dark vergence bias (Leibowitz et al., this volume). Besides relating ‘illusory concomitant motion’ to the dark-vergence bias, Post and Leibowitz’s analysis also emphasizes a basic aspect of oculomotor control that is often neglected by efference-based theories of space perception. The extraocular muscles receive innervation from multiple sources, which have evolved to serve different functions, and these separate control processes can have dissociable perceptual consequences. In general, efferent signals arising from ‘voluntary’ control centers influence perception directly, while those from lower-order systems, such as the optokinetic and vestibulo-ocular reflexes, do not affect perception. Such processes can affect perception indirectly, however, because they can modify the activity required of voluntary eye movement systems. I shall return to this point when discussing the effects of vergence on space perception.
D.A. Owens / Oculomotor tonus and visual adaptation
221
3. Parallels in oculomotor and perceptual adaptation Wallach and his colleagues have demonstrated that the relation between oculomotor adjustments and space perception is quite plastic. They found, for example, that viewing through negative lenses and base-out prisms, which force subjects to accommodate and converge ‘nearer’than usual, produced adaptive changes in perceived size, depth, and distance (Wallach and Frey 1972; Wallach et al. 1972). Wearing such spectacles initially caused objects to appear nearer and smaller than normal, but perception soon returned to normal. Upon removal of the spectacles, their subjects exhibited negative aftereffects, overestimating size, depth, and distance. Wallach et al. interpreted these results as a ‘recalibration of the relation between oculomotor adjustment and registered distance’ (1972: 116). In view of the correlation between dark vergence and the SDT, we investigated whether the resting state of the eyes might also be related to perceptual adaptation (Owens and Leibowitz 1980). This problem presented an opportunity to look more closely at the apparent dissociation of the resting states of accommodation and vergence, and it allowed us to examine a new question: what are the effects of the subjects’activities during exposure to the experimental glasses on the adaptation process? Earlier research had shown that active experience in a bright environment greatly facilitates adaptation to laterally displacing prisms (Held 1965; Welch 1978), suggesting the involvement of processesthat mediate sensorimotor coordination. Another hypothesis, appealing for its simplicity, proposed that adaptation results from changes in extraocular muscle, similar to posttetanic potentiation, which are induced by unusual or sustained effort (Ebenholtz and Wolfson 1975). In hopes of clarifying this adaptive process, we tested the effects of exposure to base-out prisms and negative lenses on both distance perception and the resting state of the eyes. A sample of 60 subjects was divided into three groups, who performed different activities during a 20-min exposure period. One group, called the ‘Walkers’, participated in a variety of complex visuomotor activities during adaptation; a second group, the ‘Riders’, rode a wheelchair over the same course as the Walkers and did not participate in the visuomotor tasks; and a third group, the ‘Readers’, remained seated in a dark room, reading an illuminated magazine at a fixed distance. Before and after
222
D.A. Owens / Oculomotor tonus and visual aduptution
the exposure period, we tested each subject’s dark focus, dark vergence, and perceived distance, measured by ‘open-loop’ pointing to a point of light viewed binocularly in the dark. The results provided further evidence that accommodation and vergence dissociate at rest, and that adaptive changes of distance perception are accompanied by parallel changes in vergence tonus. Comparison of preadaptation measures of the dark focus and dark vergence showed (1) that the mean resting positions of accommodation and vergence correspond to significantly different distances (76 and 116 cm, respectively), and (2) that the resting states of individual subjects are only weakly correlated (r = 0.32). Moreover, exposure to the experimental spectacles modified the dark vergence posture but had no effect on dark focus (fig. 4). The dark vergence of both the Walkers and the Riders exhibited a significant convergent shift, while that of the Readers showed a similar but non-significant shift. These shifts in dark vergence were accompanied by parallel changes in distance perception in low light (fig. 5). After exposure, perceived distance of both the Walkers and Riders increased significantly, and again the Readers showed a similar but non-significant change. These data replicated earlier findings that adaptation to base-out prisms and lenses produces subsequent overestimation of distance (Wallach et al. 1972; Von Hofsten 1979). Of greater interest, they indicated that this perceptual adaptation may be related to changes in vergence tonus. Parallel variations of perception and muscle tone were predicted by the eye-muscle potentiation hypothesis, which explained perceptual aftereffects in terms of peripheral neuromuscular changes produced by unusual effort. But the differential effects of activity during exposure seemed to contradict this viewpoint. According to the muscle potentiation hypothesis, greater aftereffects should be exhibited by subjects who exert greater convergence effort. Since the Readers were required to do a near task throughout the exposure period, they should have experienced greater muscle potentiation and, therefore, greater perceptual aftereffects than the Walkers and Riders, who fixated relatively distant stimuli during exposure. Our data showed the opposite outcome; adaptive changes were greater for Walkers and Riders than for Readers. This seemed more compatible with the view that adaptation involves higher processes that mediate sensorimotor coordination. But theories proposing perceptual recalibration had not considered the possible involvement of processes such as muscle tone.
D.A. Owens / Oculomotor tomu and visual rrduptution
224
D.A. Owens / Oculomotor tonus and visual adaptution
Walkers Ri’ders Readers
X---X @--a H /’
&--L.c-
/-- 0 -x
I 10
20 Distance
30 (cm)
40
Fig. 5. Changes of perceived distance for a point of light viewed in darkness after adaptation to base-out prisms and negative lenses. Perceived distance aftereffects for the three exposure conditions paralleled changes in dark vergence (fig. 4). Reprinted from Owens, D.A. and H.W. Leibowitz, 1980. Accommodation convergence, and distance perception in low illumination. American Journal of Optometry and Physiological Optics 57(9), p. 548. Copyright (1980) by the American Academy of Optometry.
4. Tonus, effort, and perception: a working hypothesis The fact that the eyes normally adjust to an intermediate distance at rest suggested a new approach to prism adaptation, and to the more general question of how oculomotor activity is related to space perception. Several earlier investigators had proposed that distance perception is influenced by the oculomotor effort required for fixation (e.g., Von Holst 1954; Leibowitz and Moore 1966; Von Hofsten 1976). The insight emerging from our experiments was that oculomotor effort, and its perceptual consequences, should be defined relative to the individual’s characteristic resting posture. This, in turn, suggested that the resting state may serve as a ‘set point’ for calibrating the effects of oculomotor effort on perception. The dark vergence posture is assumed to be the physiological resting state of the vergence system. Accordingly, it is thought to represent the starting point for active responses, and to correspond to a basic ‘reference distance’ for space perception. Fixating a target at the dark vergence distance requires no vergence effort, and the target is there-
D.A. Owens / Oculomotor
2. ADD
1. NORMAL Vergence
‘FARTHER”
I ’
I
REFERENCE
3ESTING
4. AFTEREFFECTS
3. ADAPTATION
TONUS
PRISMS
Percept ion
DIVERGENCE
RESTING
225
toma und visual uduptution
Obrects
appear
?ESTING
TONUS
I , ;
Objects
appear
tarther
an* larger
Fig. 6. Interpretation of perceptual and motor adaptation to base-out prisms based on the assumptionsthat the resting tonus corresponds to a constant perceptual ‘reference distance’, while active divergence and convergence effort produce increased and decreased perceived distance, respectively.Reprinted from Owens, D.A., in press, ‘Oculomotor information and perception of three-dimensional space’. In: H. Heuer and A.F. Sanders (eds.), Perspectives on perception ‘and action. Hillsdale, NJ: Erlbaum.
fore perceived to be at the ‘reference distance’ (fig. 6A). Fixation of stimuli nearer than the dark vergence distance requires convergence effort, however, which gives rise to perception of ‘nearer’ distance.
226
D.A. Owens / Oculomotor tonus and visual aduptution
Conversely, fixation of stimuli beyond the dark vergence distance requires divergence effort, which gives rise to perception of ‘farther’ distance (Owens, in press). Modification of the usual relation between vergence angle and fixation distance has three closely related effects. Base-out prisms, for example, deviate the visual axes in the temporal direction so that the dark vergence posture corresponds to a greater distance than usual, and consequently, the vergence effort required to fixate any binocular stimulus is altered. With the prisms in place, the resting position lies beyond the perceptual ‘reference’ distance (fig. 6B); less divergence effort is needed to fixate distant stimuli, and greater convergence effort to fixate near stimuli. These changes all have the same effect: they cause the observer to underestimate distance. Adaptation to the prisms induces a convergent shift of the dark vergence posture, which tends to restore the original relation between fixation distance, vergence effort, and perception (fig. 6C). In effect, the dark vergence posture moves toward its original fixation distance, counteracting the effect of the prisms on vergence effort. Now when viewing through the prisms, the subject’s resting position again matches the perceptual reference distance. Usual levels of vergence effort are required to fixate different distances, and this effort is again a veridical source of distance information. When the prisms are removed, however, the new calibration is no longer veridical. The resting posture now corresponds to a distance nearer than the perceptual reference distance. Therefore, greater divergence effort is needed to fixate distant stimuli, and less convergence effort is needed to fixate near stimuli (fig. 6D). As a result, the subject overestimates distance. Like Post and Leibowitz’s (1982) analysis of efferent factors in motion perception (Leibowitz et al., this volume), the present argument rests upon a distinction among multiple sources of oculomotor efference. The more familiar type of vergence efference might be called ‘active’ vergence. Its two components, divergence and convergence, utilize control input from binocular fusional processes and the accommodative system (Owens and Leibowitz 1983). As with pursuit eye movements, active vergence is initiated by voluntary effort to fixate an object, and it has a direct effect on perception. The second, less familiar type of vergence efference is the resting activity referred to as ‘dark’ or ‘tonic’ vergence. This represents the balance point between spontaneous activity of the opponent divergence and convergence
D.A. Owens / Oculomotor tonus and visual adaptation
221
systems, serving primarily for postural control. Like the gaze stability reflexes, vergence tonus is involuntary and has no direct effect on space perception. As we have seen, it can affect perception indirectly, however, because it determines the active vergence effort required to fixate an object.
5. Relevance to visual fatigue This viewpoint has also introduced a new approach to the problem of visual fatigue. Printers, office workers, and grandmothers have long believed that near work can lead to visual problems, including ‘eyestrain’ and myopia. As early as 1713, Ramazinni reported that prolonged near work produces ‘weakness of vision’ and changes in the ‘tonus of ocular filaments’. Increasing use of video display terminals (VDT’s) has caused a resurgence of interest in visual problems related to near work (Brown et al. 1982). Yet, despite the widespread belief that near work is stressful and potentially deleterious to vision, there is little scientific evidence for this claim, much less for the responsible mechanisms (National Academy of Science 1983). One of the more puzzling aspects of visual fatigue, particularly that related to VDT’s, is the fact that some people complain of severe symptoms, while others experience little or no problem. These individual differences are not predictable from standard clinical assessment, but they may be related to differences in the resting state of the eyes. Near work obviously involves oculomotor effort. Perhaps less effort is required of individuals whose eyes rest at a distance similar to the visual task. Karen Wolf and I (1983) have begun to investigate this hypothesis, and preliminary findings indicate that the individual’s resting state is a key factor. We found that reading can induce significant changes in both the dark focus and dark vergence postures, and the magnitude of such changes depends on the subject’s initial resting state. Subjects who begin with a relatively distant resting state generally show a large shift toward a nearer resting posture after reading, while those who begin with a relatively near resting state show little or no change. Since the dark focus and dark vergence postures are not closely correlated, many subjects exhibit differential changes, which allowed us to look for fatigue effects that are related specifically to accommo-
228
D.A. Owens / Oculomotor tonus and oisual uiqtution
dation or vergence. Changes in dark focus and dark vergence were correlated with dissociable symptoms of fatigue. Reading-induced shifts of the dark focus are accompanied by myopic focusing responses for bright stimuli, which can degrade acuity and may contribute to the development of myopia (Ebenholtz 1983). These changes are not related to subjective feelings of eyestrain, however (rho = 0.13). In contrast, reading-induced shifts of dark vergence are significantly correlated with subjective ratings of eyestrain (rho = 0.58), though not to changes in visual resolution. Further work is necessary to determine whether dissociable changes of accommodation and vergence have interactive effects or long-term consequences. Recognition of individual differences in the resting state of the eyes can help to clarify the nature of visual fatigue.
6. Theoretical implications While oculomotor tonus appears to be of considerable functional significance, its physiological basis is still obscure. Research on extraocular muscle has revealed slow-responding ‘tonus bundles’, not found elsewhere in mammalian muscles (Granit 1970; Burian and Von Noorden 1974). These slow-acting fibers are innervated by small-diameter (gamma range) neurons, whose activity could be dependent partly on proprioceptive feedback from the eye muscles themselves (Granit 1970, 1971; Steinbach, this volume). This possibility suggests a mechanism for the potentiation-like effects induced by unusual oculomotor effort. Near work, for example, may induce a shift of tonus through peripheral feedback from muscle receptors. Such modulation of tonus could have the advantage of reducing the effort required for the near task, thus increasing control efficiency. It is not clear that such peripherally mediated changes would be advantageous for perception, nor that tonus is determined entirely by such peripheral feedback. Behavioral studies have shown that adaptation is not always predicted by induction effort (Heuer, this volume), and it is often enhanced by perceptual-motor discrepancies (fig. 4; Wallach and Halpern 1977). These findings imply that tonus is also dependent on more central mechanisms which mediate sensorimotor coordination. This sort of hierarchical control of vergence tonus would not be unusual in the context of motor control theory. To the contrary,
D.A. Owens / Oculomotor tonus and visual adaptation
229
multiple levels of control, including automatic peripheral ‘servo-mechanisms’and higher-level selection, guidance, and coordination, are typical of the control of both posture and locomotion (Granit 1970). While the present interpretation extends well beyond the available data, it is appealing for several reasons. It is consistent with our knowledge of motor control and oculomotor physiology, yet it requires many changes in our notions of how accommodation and vergence work, and how they affect perception. Understanding that the eyes rest at an intermediate rather than an extreme position in their operating range, and that the resting posture exhibits wide individual differences, helps to explain why perception is so imprecise and varies so widely among subjects under low visibility conditions. It also provides a simple framework for explaining the role of oculomotor efference in perception and perceptual adaptation without resource to mentalistic computations or to memory-intensive learning processes. Further investigation may show it to be equally illuminating for problems of visual fatigue and for clinical phenomena such as the sensorimotor adaptation exhibited by some strabismic patients (Campos, this volume). Perhaps oculomotor tonus is what Turvey (this volume) is referring to when he recommends that we look for ‘states that perceiving-acting systemsrelax onto and regulate around’. In any event, it appears to be helpful in understanding oculomotor behavior and its influence on perception.
References Baird, J.W., 1903. The influence of accommodation and convergence upon the perception of depth. American Journal of Psychology 14, 150-200. Berkeley,G., 1709. ‘An essay towards a new theory of vision’. In: A.D. Lindsay (ed.), Berkeley: a new theory of vision and other writings. London: J.M. Dent & Sons, 1972. Brown, B.S., K. Dismukes and E.J. Kinalducci, 1982. Video display terminals and vision of workers: summary and overview of a symposium. Behavior and Information Technology 1, 121-140. Burian, H.M. and G.K. von Noorden, 1974. Binocular vision and ocular motility. St. Louis, MO: C.V. Mosby. Campos, E.C., 1986. Sensory and sensori-motor adaptations in strabismus: their role in space perception. Paper presented at the conference on Sensorimotor Interactions in Space Perception and Action, University of Bielefeld, Febr. 1985. Acta Psychologica 63, 281-295 (this volume). Cogan, D.G., 1937. Accommodation and the autonomic nervous system. Archives of Ophthalmology 18,139-766.
230
D.A. Owens / Oculomotor tonuS and visual adaptation
Cornelius, C.S., 1861. Die Theorie des Sehens und rlumlichen Vorstellens. Halle: H.W. Schmidt. pp. 283-285. Descartes, R., 1664. ‘Le monde. Trait& de l’homme’. In: C. Adam and P. Tannery (eds.), Oeuvres de Descartes, Vol. XI. Paris: Librarie Philosophie J. Vrin, 1967. pp. 155-161, 183-185. Ebenholtz, SM., 1983. Accommodative hysteresis: a precursor for induced myopia? Investigative Ophthalmology & Visual Science 24, 513-515. Ebenholtz, SM. and D.M. Wolfson, 1975. Perceptual aftereffects of sustained convergence. Perception and Psychophysics 17, 485-491. Fincham, E.F., 1962. Accommodation and convergence in the absence of retinal images. Vision Research 1, 425-440. Foley, J.M., 1980. Binocular distance perception. Psychological Review 87, 411-434. Francis, E.L. and D.A. Owens, 1983. The accuracy of binocular vergence for peripheralstimuli. Vision Research 23, 13-19. Gogel, W.C., 1969. The sensing of retinal size. Vision Research 9, 1079-1094. Gogel, W.C., 1977. ‘The metric of visual space’. In: W. Epstein (ed.), Stability and constancy in visual perception: mechanisms and processes. New York: Wiley. Granit, R., 1970. The basis of motor control. New York: Academic Press. Granit, R., 1971. ‘The probable role of muscle spindles and tendon organs in eye movement control’. In: P. Bach-y-Rita and C.C. Collins (eds.), The control of eye movements. New York: Academic Press. Held, R., 1965. Plasticity in sensory-motor systems. Scientific American 213, 84-94. Helmholtz, H., 1867. Handbuch der physiologischen Optik. Leipzig: Voss. (Or see English trans. of 3rd ed., by later workers, by J.P.C. Southall, New York: Dover, 1962.) Hennessy, R.T. and H.W. Leibowitz, 1972. Laser optometer incorporating the Badal principle. Behavior Research Methods and Instrumentation 4, 237-239. Heuer, H., 1986. Perceptual aftereffects of sustained fixation and oculomotor changes. Paper presented at the conference on Sensorimotor Interactions in Space Perception and Action, University of Bielefeld, Febr. 1985. Acta Psychologica 63, 247-261 (this volume). Ivanoff, A. and C. Bourdy, 1954. Le comportement de la convergence en nocturne [The behavior of convergence in night vision.] Ann Optique Oculaire 3, 70-75. (Eng. trans available from DAO.) Leibowitz, H.W. and D. Moore, 1966. Role of changes in accommodation and convergence in the perception of size. Journal of the Optical Society of America 56, 1120-1123. Leibowitz, H.W. and D.A. Owens, 1978. New evidence for the intermediate position of relaxed accommodation. Documenta Ophthalmologica 46, 133-147. Leibowitz, H.W., R.B. Post and J. Sheehy, 1986. Efference, perceived movement, and illusory displacement. Paper presented at the conference ,on Sensotimotor Interactions in Space Perception and Action, University of Bielefeld, Febr. 1985. Acta Psychologica 63, 23-34 (this volume). Maddox, E.E., 1893. The clinical use of prisms: and the decentering of lenses, 2nd ed. Bristol: John Wright. Morgan, M.W., 1946. A new theory for the control of accommodation. American Journal of Optometry 23, 99-110. Morgan, M.W., 1968. Accommodation and vergence. American Journal of Optometry 45,415-454. National Academy of Science, 1983. Video displays, work, and vision. Washington, DC: National Academy Press. Owens, D.A., 1984. The resting state of the eyes. American Scientist 72, 378-387. Owens, D.A., in press. ‘Oculomotor information and perception of three-dimensional space’. In: H. Heuer and A.F. Sanders (eds.), Perspectives on perception and action. Hillsdale, NJ: Erlbaum.
D.A. Owens / Oculomotor tonus and visuul uduptation
231
Owens, D.A. and H.W. Leibowitz, 1976. Oculomotor adj,ustments in darkness and the specific distance tendency. Perception and Psychophysics 20, 2-9. Owens, D.A. and H.W. Leibowitz, 1980. Accommodation, convergence, and distance perception in low illumination. American Journal of Optometry and Physiological Optics 57, 540-550. Owens, D.A. and H.W. Leibowitz, 1983. ‘Perceptual and motor consequences of tonic vergence’. In: C. Schor and K. Ciuffreda (eds.), Vergence eye movements: basic and clinical aspects. Boston, MA: Butterworths. Owens, D.A. and K.S. Wolf, 1983. Accommodation, binocular vergence, and visual fatigue. Investigative Ophthalmology & Visual Science (Suppl.) 24, 23. Post, R.B. and H.W. Leibowitz, 1982. The effect of convergence on the vestibule-ocular reflex and implications for perceived movement. Vision Research 22, 461-465. Ramazinni, B., 1713. Diseases of workers. Eng. trans. by W.C. Wright. Chicago, IL: University of Chicago, 1940. pp. 323-325, 415-419. Schober, H., 1954. Uber die Akkommodationsruhelage. Optik 6, 282-290. (Eng. trans. available from DAO.) Steinbach, M.J., 1986. Inflow as a long-term calibrator of eye position in humans. Acta Psychologica 63,297-306 (this volume). Based on’Behaviora1 and anatomical evidence for eye muscle proprioception in surgically-treated humans. Paper presented at the conference on Sensorimotor Interactions in Space Perception and Action, University of Bielefeld, Febr. 1985. Swenson,H.A., 1932. The relative influence of accommodation and convergence in the judgement of distance. Journal of General Psychology, 7, 360-379. Turvey, M.T. and C. Carello, 1986. The ecological approach to perceiving-acting: a pictorial essay. Acta Psychologica 63, 133-155 (this volume). Based on Optical basis of controlled collisions. Paper presented at the conference on Sensorimotor Interactions in Space Perception and Action, University of Bielefeld, Febr. 1985. Von Hofsten, C., 1976. The role of convergence in visual space perception. Vision Research 16, 193-198. Von Hofsten, C., 1979. Recalibration of the convergence system. Perception 8, 37-42. Von Holst, E., 1954. Relations between the central nervous system and the peripheral organs. British Journal of Animal Behaviour 2, 89-94. Wallach, H. and K.J. Frey, 1972. Adaptation in distance perception based on oculomotor cues. Perception & Psychophysics 11, 77-83. Wallach, H. and P. Halpern, 1977. Eye muscle potentiation does not account for adaptation in distance perception based on oculomotor cues. Perception & Psychophysics 22, 427-430. Wallach, H., K.J. Frey and K.A. Bode, 1972. The nature of adaptation in distance perception based on oculomotor cues. Perception and Psychophysics 11, 110-16. Welch, R.B., 1978. Perceptual modification: adapting to altered sensory environments. New York: Academic Press. Wundt, W., 1862. Beitrlge zur Theorie der Sinneswahrnehmung. Heidelberg: CF. Winter’sche Verlagshandlung.
OCULQMOTOR
TONUS AND VISUAL
213
ADAPTATION
*
D. Alfred OWENS Franklin & Marshall College, Lmzcaster, USA Accepted March 1986
The contribution of oculomotor efference to visual perception and performance can be clarified by considering the functions of tonus. Accommodation and vergence typically ‘relax’ at an intermediate distance, reflecting tonic innervation of the ciliary and extraocular muscles, which varies widely among individuals who have normal vision. In many situations, especially when stimulation is degraded, fixation and focusing responses are biased toward the individual’s resting state. Moreover, unusual circumstances, such as alteration of the relation of eye position and distanceor prolonged exposure to near work, induce adaptive modification of the resting posture. Thesenormal variations of oculomotor tonus affect the accuracy and the effort required to fixate objects,and they may help explain problems of space perception and visual fatigue.
1. Introduction This paper examines the role of oculomotor tonus in two phenomena that have a long history in the study of vision. The first, which is somewhat closer to the issue of perceiving three-dimensional space, concernsthe manner in which accommodation and vergence eye movements affect distance perception. The second, which is more closely related to acting in three-dimensional space, concerns the contribution of oculomotor processes to symptoms of visual fatigue. Following traditional theories (Helmholtz 1867; Maddox 1893), previous inquiries into both of these problems have assumed that accommodation and * This paper is based on a presentation at the Conference on Sensorimotor Interactions in Space Perception and Action at the Zentrum fir interdisziplinlre Forschung (ZiF) der UniversitPt Bielefeld in February, 1985. I want to thank Annie Vinter for helping to translate Descartes. Preparation of this paper was supported by ZiF and Franklin & Marshall College; the research wassupported in part by Grant EY-03898 from the National Eye Institute. Mailing address: D.A. Owens, Whitely Psychology Laboratories, Franklin & Marshall College, P.O.Box 3003, Lancaster, PA 17604-3003, USA. OoOl-6918/86/$3.50 0 1986, Elsevier Science Publishers B.V. (North-Holland)
214
D.A. Owens / Oculomotor tonus und visual adapotion
vergence adjust to optical infinity at rest. We now know this is not the case (Owens 1984). Rather, both systems adopt intermediate postures at rest. Abandoning the old view requires a new conception of the processes controlling accommodation and vergence and of their functional impact on perception and performance. It introduces a new approach to perceptual problems that arise under low visibility conditions, and it suggests a new interpretation of the adaptive changes found with exposure to effortful visual tasks and with alterations of the relation of eye position and environmental space.
2. Accommodation, vergence, and distance perception One of the oldest hypotheses in the literature on vision is that eye position, particularly binocular vergence, provides information about the location of objects in space. Descartes (1664) argued that we have the innate capacity to sense the angle of convergence and ‘compute’, by some sort of unconscious geometry, the distance of fixated objects. He was also the first to describe accurately the mechanism of visual accommodation and to propose that accommodative, as well as vergence, responses contribute to distance perception (fig. 1). Although Descartes’ theory did not survive intact, the notion that distance perception depends at least partly on vergence and accommodation did. Berkeley (1709) argued that, while it is absurd to explain distance perception in terms of innate geometric ideas that are quite inaccessible to conscious awareness, it is reasonable to assume that we acquire oculomotor information about distance through the association of eye-muscle sensations with distance sensations provided by tactual interactions with the environment. His work may be the clearest early statement of the theory that we must learn to perceive three-dimensional space and that ‘the hand educates the eye’. These ideas were inherited by experimental psychology and soon began to lose credibility. The experimental evidence collected by Wundt (1862), Helmholtz (1867), Baird (1903) and many others showed that people do not perceive depth and distance as accurately as the philosophers had supposed, at least not under laboratory conditions designed to isolate oculomotor information. While the results and interpretations varied, the evidence was fairly consistent on two points: (1) binocular judgements are more accurate than monocular observations, although
Fis. lb.
Fig. 1. Descartes’ (1664) sketches of oculomotor mechanisms of distance perception. Fig. 11 illustrates his accurate model of visual accommodation: the crystalline lens must assume shapes ‘I’ and ‘F’ to focus distances ‘X’ and ‘T’, respectively. Vergence angle and distance (fig. 16) were thought to be perceived by innate geometry, just as the blind man (fig. 15) perceives the angles and distance of the intersecting sticks. Reprinted from Descartes, R., 1664. ‘Le monde. Trait& de l’homme’. In: C. Adam and P. Tannery (eds.), Oeuvres de Descartes, Vol. XI, Paris: Librairie Philosophie J. Vrin, 1967. pp. 155-162.
Pip. IS.
c: VI
216
D.A. Owens / Oculomotor tonus and visual aduptation
neither are very accurate; (2) subjects vary widely in their errors, with some tending to underestimate distance (e.g., Wundt 1862), and others tending to overestimate distance (e.g., Hehnholtz 1867). The poor accuracy and high variability of such data contributed to the view that oculomotor information is less effective than ‘pictorial cues’ for distance. A common finding of studies of space perception under ‘reduced cue’ conditions, is that judgements of size and distance tend to be biased toward a distance of 1 or 2 meters (Swenson 1932; Foley 1980). This perceptual bias was studied most extensively by Gogel (1969, 1977) who referred to the phenomenon as the ‘specific distance tendency’ (SIP). According to Gogel, the SDT represents an ‘autochthonic’ perceptual bias that operates in combination with pictorial and oculomotor cues to determine perceived distance. The influence of the SDT increases as other information decreases. Therefore, it is best measured in conditions devoid of distance information, as with a small luminous target viewed monocularly in darkness. Such measures show considerable intersubject variability, with SDT values ranging from about 30 cm to several meters. The SDT was an appealing concept because it explained a variety of spatial illusions in terms of a common process, a systematic bias of perceived distance under reduced stimulus conditions. At the same time, this concept raised new questions about why perception is biased toward an intermediate distance, ,and why this bias exhibits such wide individual differences. New research on accommodation provided a clue to the possible basis of the SDT. The development of the laser-Badal optometer (Hennessy and Leibowitz 1972) allowed measurement of ocular refraction without stimulating accommodation, enabling us to reexamine an old controversy about the resting state of accommodation. As noted earlier, popular theories claimed that the eyes relax at the far point of their operating range. Accordingly, oculomotor effort was thought to be necessary only to see near stimuli, while passive forces (such as elasticity of supporting tissues) were thought to shift focus and fixation from near to distant stimuli. This view was not unanimous, however. Over the past 130 years it has been challenged by several authors, who proposed instead that accommodation relaxes at an intermediate distance (Weber 1855, .cited by Cornelius 1861; Cogan 1937; Morgan 1946; Schober 1954). The intermediate resting state hypothesis was appealing because (1) it implied that accommodation, like most other
D.A. Owens / Oculomotor tonus and visual adaptation
217
motor systems, is comprised of opponent (near and far) mechanisms, and (2) it offered a simple explanation for ‘anomalous myopias’ that appear under reduced stimulus conditions and seem paradoxical from the traditional viewpoint (Leibowitz and Owens 1978). There were few data to support this novel hypothesis, however, and it had little impact on mainstream theory and practice. Early studies with the laser optometer provided new evidence for the intermediate resting state hypothesis. Measurements of the ‘dark focus’ showed that most subjects accommodate to an intermediate distance in darkness. They also revealed unexpectedly wide variability among subjects with normal vision. One large sample yielded individual dark focus values ranging from infinity to 4 diopters (D; 25 cm), with an average of 1.5 D, or 67 cm (fig. 2A). Furthermore, measures taken under a wide variety of conditions showed that focusing responses for visible targets are often biased toward the subject’s dark focus, especially under degraded stimulus conditions (Leibowitz and Owens 1978). So the laser optometer not only revived the intermediate resting state hypothesis, but also provided a new insight regarding normal variations of the behavior of accommodation. The operating range of accommodation depends on the strength of available stimulation (fig. 2B). Whenever stimulation is reduced, subjects generally become increasingly myopic for distant stimuli and hyperopic for near stimuli. These normal variations of accommodation suggested an alternative explanation for the SDT. Conditions used to measure the SDT provided little or no feedback for accommodation. Therefore, subjects would most likely focus for an intermediate distance, and this bias might influence distance perception. A comparison of the dark focus and the SDT showed no relationship, however. Although both the average dark focus and SDT values corresponded to intermediate distances (41 and 145 cm, respectively) the measures of individual subjects were not significantly correlated (fig. 3A). While this finding ruled out the hypothesis that the SDT results from errors of accommodation, it did not eliminate the possible involvement of binocular vergence. This possibility seemed unlikely at first because vergence and accommodation are normally closely correlated (Morgan 1968). We therefore assumed they would adjust to the same distance at rest. As with accommodation, traditional theories of vergence held that the eyes return to a parallel or slightly divergent position at rest (Maddox 1893). But later work showed that vergence
D.A. Owens / Oculomotor tonus and visual adaptation
218
30
N=220 Mean = 1.52 SD. = 0.77
25 20
r
15 10 5
33
25
cm
FCCUS IN DARKNESS 5 -B 2 al --5
Strong
4 =
Stimulation
I $ ti “,i Lrl a
D E
Weaker
:
2.
3-
i
: a ‘; 2 xl
1 -
No Stimulation
5
0
0 M
I 100
2 50
STIMULUS (cm and diopters
3 33
4 25
Stimulation
5
D-MA
20
cm
DISTANCE
or meter-angles.
D-MA)
Fig. 2. (A) Distribution of dark focus values of 220 college students. Contrary to classical theory, the resting focus corresponds to an intermediate distance and shows wide intersubject variability. (B) As stimulation is degraded, accommodation and vergence responses are progressively biased toward the observer’s resting posture. This bias typically results in increasing ‘myopic’ or ‘esophotic’ errors for distant targets and increasing ‘hyperopic’ or ‘exophoric’ errors for near targets. Fig. 2A reprinted from Leibowitz, H.W. and D.A. Owens, 1978. New evidence for the intermediate position of relaxed accommodation. Documenta Ophthalmologica 46, p. 136; fig. 2B reprinted from Owens, D.A., in press. ‘Oculomotor information and perception of three-dimensional space’. In: H. Heuer and A.F. Sanders (eds.), Perspectives on perception and action. Hillsdale, NJ: Erlbaum.
D.A. Owens / Oculomotor tonus und visual adaptation
m
219
220
D.A. Owens / Oculomotor tows and visuul adaptation
also shifts toward an intermediate posture when illumination is reduced (Ivanoff and Bourdy 1954). Moreover, one study had reported that vergence and accommodation dissociate ‘in the absence of retinal images’ (Fincham 1962). This suggested that they might rest at different distances. If so, then the SDT might be related to vergence rather than to accommodation. We tested this hypothesis in a second experiment which compared subjects’ SDT with their ‘dark vergence’ posture (Owens and Leibowitz 1976). This time the data showed a significant correlation (fig. 3B). So it appeared that, although the dark focus has little or no effect on space perception, dark vergence posture is related to distance perception in low illumination. This correlation does not necessarily mean that the SDT is caused by dark vergence, but it does suggest that spatial illusions encountered under degraded visual conditions are related to vergence behavior. This interpretation was reinforced by two subsequent studies. In an investigation of vergence for dim peripheral stimuli, Ellie Francis and I (1983) found that, as stimulus eccentricity increases, responses are increasingly biased toward the observer’s dark vergence posture. Thus, like the dark focus bias, vergence responses are progressively biased toward the resting position as disparity information is degraded (fig. 2B). In another study, Post and Leibowitz (1982) found that ‘illusory concomitant motion’, which can occur with head movements in low illumination, results from an anomalous interaction between voluntary pursuit and reflexive eye movement systems. They traced this phenomenon to inappropriate ‘gain’ of the vestibulo-ocular reflex, which results from the dark vergence bias (Leibowitz et al., this volume). Besides relating ‘illusory concomitant motion’ to the dark-vergence bias, Post and Leibowitz’s analysis also emphasizes a basic aspect of oculomotor control that is often neglected by efference-based theories of space perception. The extraocular muscles receive innervation from multiple sources, which have evolved to serve different functions, and these separate control processes can have dissociable perceptual consequences. In general, efferent signals arising from ‘voluntary’ control centers influence perception directly, while those from lower-order systems, such as the optokinetic and vestibulo-ocular reflexes, do not affect perception. Such processes can affect perception indirectly, however, because they can modify the activity required of voluntary eye movement systems. I shall return to this point when discussing the effects of vergence on space perception.
D.A. Owens / Oculomotor tonus and visual adaptation
221
3. Parallels in oculomotor and perceptual adaptation Wallach and his colleagues have demonstrated that the relation between oculomotor adjustments and space perception is quite plastic. They found, for example, that viewing through negative lenses and base-out prisms, which force subjects to accommodate and converge ‘nearer’than usual, produced adaptive changes in perceived size, depth, and distance (Wallach and Frey 1972; Wallach et al. 1972). Wearing such spectacles initially caused objects to appear nearer and smaller than normal, but perception soon returned to normal. Upon removal of the spectacles, their subjects exhibited negative aftereffects, overestimating size, depth, and distance. Wallach et al. interpreted these results as a ‘recalibration of the relation between oculomotor adjustment and registered distance’ (1972: 116). In view of the correlation between dark vergence and the SDT, we investigated whether the resting state of the eyes might also be related to perceptual adaptation (Owens and Leibowitz 1980). This problem presented an opportunity to look more closely at the apparent dissociation of the resting states of accommodation and vergence, and it allowed us to examine a new question: what are the effects of the subjects’activities during exposure to the experimental glasses on the adaptation process? Earlier research had shown that active experience in a bright environment greatly facilitates adaptation to laterally displacing prisms (Held 1965; Welch 1978), suggesting the involvement of processesthat mediate sensorimotor coordination. Another hypothesis, appealing for its simplicity, proposed that adaptation results from changes in extraocular muscle, similar to posttetanic potentiation, which are induced by unusual or sustained effort (Ebenholtz and Wolfson 1975). In hopes of clarifying this adaptive process, we tested the effects of exposure to base-out prisms and negative lenses on both distance perception and the resting state of the eyes. A sample of 60 subjects was divided into three groups, who performed different activities during a 20-min exposure period. One group, called the ‘Walkers’, participated in a variety of complex visuomotor activities during adaptation; a second group, the ‘Riders’, rode a wheelchair over the same course as the Walkers and did not participate in the visuomotor tasks; and a third group, the ‘Readers’, remained seated in a dark room, reading an illuminated magazine at a fixed distance. Before and after
222
D.A. Owens / Oculomotor tonus and visual aduptution
the exposure period, we tested each subject’s dark focus, dark vergence, and perceived distance, measured by ‘open-loop’ pointing to a point of light viewed binocularly in the dark. The results provided further evidence that accommodation and vergence dissociate at rest, and that adaptive changes of distance perception are accompanied by parallel changes in vergence tonus. Comparison of preadaptation measures of the dark focus and dark vergence showed (1) that the mean resting positions of accommodation and vergence correspond to significantly different distances (76 and 116 cm, respectively), and (2) that the resting states of individual subjects are only weakly correlated (r = 0.32). Moreover, exposure to the experimental spectacles modified the dark vergence posture but had no effect on dark focus (fig. 4). The dark vergence of both the Walkers and the Riders exhibited a significant convergent shift, while that of the Readers showed a similar but non-significant shift. These shifts in dark vergence were accompanied by parallel changes in distance perception in low light (fig. 5). After exposure, perceived distance of both the Walkers and Riders increased significantly, and again the Readers showed a similar but non-significant change. These data replicated earlier findings that adaptation to base-out prisms and lenses produces subsequent overestimation of distance (Wallach et al. 1972; Von Hofsten 1979). Of greater interest, they indicated that this perceptual adaptation may be related to changes in vergence tonus. Parallel variations of perception and muscle tone were predicted by the eye-muscle potentiation hypothesis, which explained perceptual aftereffects in terms of peripheral neuromuscular changes produced by unusual effort. But the differential effects of activity during exposure seemed to contradict this viewpoint. According to the muscle potentiation hypothesis, greater aftereffects should be exhibited by subjects who exert greater convergence effort. Since the Readers were required to do a near task throughout the exposure period, they should have experienced greater muscle potentiation and, therefore, greater perceptual aftereffects than the Walkers and Riders, who fixated relatively distant stimuli during exposure. Our data showed the opposite outcome; adaptive changes were greater for Walkers and Riders than for Readers. This seemed more compatible with the view that adaptation involves higher processes that mediate sensorimotor coordination. But theories proposing perceptual recalibration had not considered the possible involvement of processes such as muscle tone.
D.A. Owens / Oculomotor tomu and visual rrduptution
224
D.A. Owens / Oculomotor tonus and visual adaptution
Walkers Ri’ders Readers
X---X @--a H /’
&--L.c-
/-- 0 -x
I 10
20 Distance
30 (cm)
40
Fig. 5. Changes of perceived distance for a point of light viewed in darkness after adaptation to base-out prisms and negative lenses. Perceived distance aftereffects for the three exposure conditions paralleled changes in dark vergence (fig. 4). Reprinted from Owens, D.A. and H.W. Leibowitz, 1980. Accommodation convergence, and distance perception in low illumination. American Journal of Optometry and Physiological Optics 57(9), p. 548. Copyright (1980) by the American Academy of Optometry.
4. Tonus, effort, and perception: a working hypothesis The fact that the eyes normally adjust to an intermediate distance at rest suggested a new approach to prism adaptation, and to the more general question of how oculomotor activity is related to space perception. Several earlier investigators had proposed that distance perception is influenced by the oculomotor effort required for fixation (e.g., Von Holst 1954; Leibowitz and Moore 1966; Von Hofsten 1976). The insight emerging from our experiments was that oculomotor effort, and its perceptual consequences, should be defined relative to the individual’s characteristic resting posture. This, in turn, suggested that the resting state may serve as a ‘set point’ for calibrating the effects of oculomotor effort on perception. The dark vergence posture is assumed to be the physiological resting state of the vergence system. Accordingly, it is thought to represent the starting point for active responses, and to correspond to a basic ‘reference distance’ for space perception. Fixating a target at the dark vergence distance requires no vergence effort, and the target is there-
D.A. Owens / Oculomotor
2. ADD
1. NORMAL Vergence
‘FARTHER”
I ’
I
REFERENCE
3ESTING
4. AFTEREFFECTS
3. ADAPTATION
TONUS
PRISMS
Percept ion
DIVERGENCE
RESTING
225
toma und visual uduptution
Obrects
appear
?ESTING
TONUS
I , ;
Objects
appear
tarther
an* larger
Fig. 6. Interpretation of perceptual and motor adaptation to base-out prisms based on the assumptionsthat the resting tonus corresponds to a constant perceptual ‘reference distance’, while active divergence and convergence effort produce increased and decreased perceived distance, respectively.Reprinted from Owens, D.A., in press, ‘Oculomotor information and perception of three-dimensional space’. In: H. Heuer and A.F. Sanders (eds.), Perspectives on perception ‘and action. Hillsdale, NJ: Erlbaum.
fore perceived to be at the ‘reference distance’ (fig. 6A). Fixation of stimuli nearer than the dark vergence distance requires convergence effort, however, which gives rise to perception of ‘nearer’ distance.
226
D.A. Owens / Oculomotor tonus and visual aduptution
Conversely, fixation of stimuli beyond the dark vergence distance requires divergence effort, which gives rise to perception of ‘farther’ distance (Owens, in press). Modification of the usual relation between vergence angle and fixation distance has three closely related effects. Base-out prisms, for example, deviate the visual axes in the temporal direction so that the dark vergence posture corresponds to a greater distance than usual, and consequently, the vergence effort required to fixate any binocular stimulus is altered. With the prisms in place, the resting position lies beyond the perceptual ‘reference’ distance (fig. 6B); less divergence effort is needed to fixate distant stimuli, and greater convergence effort to fixate near stimuli. These changes all have the same effect: they cause the observer to underestimate distance. Adaptation to the prisms induces a convergent shift of the dark vergence posture, which tends to restore the original relation between fixation distance, vergence effort, and perception (fig. 6C). In effect, the dark vergence posture moves toward its original fixation distance, counteracting the effect of the prisms on vergence effort. Now when viewing through the prisms, the subject’s resting position again matches the perceptual reference distance. Usual levels of vergence effort are required to fixate different distances, and this effort is again a veridical source of distance information. When the prisms are removed, however, the new calibration is no longer veridical. The resting posture now corresponds to a distance nearer than the perceptual reference distance. Therefore, greater divergence effort is needed to fixate distant stimuli, and less convergence effort is needed to fixate near stimuli (fig. 6D). As a result, the subject overestimates distance. Like Post and Leibowitz’s (1982) analysis of efferent factors in motion perception (Leibowitz et al., this volume), the present argument rests upon a distinction among multiple sources of oculomotor efference. The more familiar type of vergence efference might be called ‘active’ vergence. Its two components, divergence and convergence, utilize control input from binocular fusional processes and the accommodative system (Owens and Leibowitz 1983). As with pursuit eye movements, active vergence is initiated by voluntary effort to fixate an object, and it has a direct effect on perception. The second, less familiar type of vergence efference is the resting activity referred to as ‘dark’ or ‘tonic’ vergence. This represents the balance point between spontaneous activity of the opponent divergence and convergence
D.A. Owens / Oculomotor tonus and visual adaptation
221
systems, serving primarily for postural control. Like the gaze stability reflexes, vergence tonus is involuntary and has no direct effect on space perception. As we have seen, it can affect perception indirectly, however, because it determines the active vergence effort required to fixate an object.
5. Relevance to visual fatigue This viewpoint has also introduced a new approach to the problem of visual fatigue. Printers, office workers, and grandmothers have long believed that near work can lead to visual problems, including ‘eyestrain’ and myopia. As early as 1713, Ramazinni reported that prolonged near work produces ‘weakness of vision’ and changes in the ‘tonus of ocular filaments’. Increasing use of video display terminals (VDT’s) has caused a resurgence of interest in visual problems related to near work (Brown et al. 1982). Yet, despite the widespread belief that near work is stressful and potentially deleterious to vision, there is little scientific evidence for this claim, much less for the responsible mechanisms (National Academy of Science 1983). One of the more puzzling aspects of visual fatigue, particularly that related to VDT’s, is the fact that some people complain of severe symptoms, while others experience little or no problem. These individual differences are not predictable from standard clinical assessment, but they may be related to differences in the resting state of the eyes. Near work obviously involves oculomotor effort. Perhaps less effort is required of individuals whose eyes rest at a distance similar to the visual task. Karen Wolf and I (1983) have begun to investigate this hypothesis, and preliminary findings indicate that the individual’s resting state is a key factor. We found that reading can induce significant changes in both the dark focus and dark vergence postures, and the magnitude of such changes depends on the subject’s initial resting state. Subjects who begin with a relatively distant resting state generally show a large shift toward a nearer resting posture after reading, while those who begin with a relatively near resting state show little or no change. Since the dark focus and dark vergence postures are not closely correlated, many subjects exhibit differential changes, which allowed us to look for fatigue effects that are related specifically to accommo-
228
D.A. Owens / Oculomotor tonus and oisual uiqtution
dation or vergence. Changes in dark focus and dark vergence were correlated with dissociable symptoms of fatigue. Reading-induced shifts of the dark focus are accompanied by myopic focusing responses for bright stimuli, which can degrade acuity and may contribute to the development of myopia (Ebenholtz 1983). These changes are not related to subjective feelings of eyestrain, however (rho = 0.13). In contrast, reading-induced shifts of dark vergence are significantly correlated with subjective ratings of eyestrain (rho = 0.58), though not to changes in visual resolution. Further work is necessary to determine whether dissociable changes of accommodation and vergence have interactive effects or long-term consequences. Recognition of individual differences in the resting state of the eyes can help to clarify the nature of visual fatigue.
6. Theoretical implications While oculomotor tonus appears to be of considerable functional significance, its physiological basis is still obscure. Research on extraocular muscle has revealed slow-responding ‘tonus bundles’, not found elsewhere in mammalian muscles (Granit 1970; Burian and Von Noorden 1974). These slow-acting fibers are innervated by small-diameter (gamma range) neurons, whose activity could be dependent partly on proprioceptive feedback from the eye muscles themselves (Granit 1970, 1971; Steinbach, this volume). This possibility suggests a mechanism for the potentiation-like effects induced by unusual oculomotor effort. Near work, for example, may induce a shift of tonus through peripheral feedback from muscle receptors. Such modulation of tonus could have the advantage of reducing the effort required for the near task, thus increasing control efficiency. It is not clear that such peripherally mediated changes would be advantageous for perception, nor that tonus is determined entirely by such peripheral feedback. Behavioral studies have shown that adaptation is not always predicted by induction effort (Heuer, this volume), and it is often enhanced by perceptual-motor discrepancies (fig. 4; Wallach and Halpern 1977). These findings imply that tonus is also dependent on more central mechanisms which mediate sensorimotor coordination. This sort of hierarchical control of vergence tonus would not be unusual in the context of motor control theory. To the contrary,
D.A. Owens / Oculomotor tonus and visual adaptation
229
multiple levels of control, including automatic peripheral ‘servo-mechanisms’and higher-level selection, guidance, and coordination, are typical of the control of both posture and locomotion (Granit 1970). While the present interpretation extends well beyond the available data, it is appealing for several reasons. It is consistent with our knowledge of motor control and oculomotor physiology, yet it requires many changes in our notions of how accommodation and vergence work, and how they affect perception. Understanding that the eyes rest at an intermediate rather than an extreme position in their operating range, and that the resting posture exhibits wide individual differences, helps to explain why perception is so imprecise and varies so widely among subjects under low visibility conditions. It also provides a simple framework for explaining the role of oculomotor efference in perception and perceptual adaptation without resource to mentalistic computations or to memory-intensive learning processes. Further investigation may show it to be equally illuminating for problems of visual fatigue and for clinical phenomena such as the sensorimotor adaptation exhibited by some strabismic patients (Campos, this volume). Perhaps oculomotor tonus is what Turvey (this volume) is referring to when he recommends that we look for ‘states that perceiving-acting systemsrelax onto and regulate around’. In any event, it appears to be helpful in understanding oculomotor behavior and its influence on perception.
References Baird, J.W., 1903. The influence of accommodation and convergence upon the perception of depth. American Journal of Psychology 14, 150-200. Berkeley,G., 1709. ‘An essay towards a new theory of vision’. In: A.D. Lindsay (ed.), Berkeley: a new theory of vision and other writings. London: J.M. Dent & Sons, 1972. Brown, B.S., K. Dismukes and E.J. Kinalducci, 1982. Video display terminals and vision of workers: summary and overview of a symposium. Behavior and Information Technology 1, 121-140. Burian, H.M. and G.K. von Noorden, 1974. Binocular vision and ocular motility. St. Louis, MO: C.V. Mosby. Campos, E.C., 1986. Sensory and sensori-motor adaptations in strabismus: their role in space perception. Paper presented at the conference on Sensorimotor Interactions in Space Perception and Action, University of Bielefeld, Febr. 1985. Acta Psychologica 63, 281-295 (this volume). Cogan, D.G., 1937. Accommodation and the autonomic nervous system. Archives of Ophthalmology 18,139-766.
230
D.A. Owens / Oculomotor tonuS and visual adaptation
Cornelius, C.S., 1861. Die Theorie des Sehens und rlumlichen Vorstellens. Halle: H.W. Schmidt. pp. 283-285. Descartes, R., 1664. ‘Le monde. Trait& de l’homme’. In: C. Adam and P. Tannery (eds.), Oeuvres de Descartes, Vol. XI. Paris: Librarie Philosophie J. Vrin, 1967. pp. 155-161, 183-185. Ebenholtz, SM., 1983. Accommodative hysteresis: a precursor for induced myopia? Investigative Ophthalmology & Visual Science 24, 513-515. Ebenholtz, SM. and D.M. Wolfson, 1975. Perceptual aftereffects of sustained convergence. Perception and Psychophysics 17, 485-491. Fincham, E.F., 1962. Accommodation and convergence in the absence of retinal images. Vision Research 1, 425-440. Foley, J.M., 1980. Binocular distance perception. Psychological Review 87, 411-434. Francis, E.L. and D.A. Owens, 1983. The accuracy of binocular vergence for peripheralstimuli. Vision Research 23, 13-19. Gogel, W.C., 1969. The sensing of retinal size. Vision Research 9, 1079-1094. Gogel, W.C., 1977. ‘The metric of visual space’. In: W. Epstein (ed.), Stability and constancy in visual perception: mechanisms and processes. New York: Wiley. Granit, R., 1970. The basis of motor control. New York: Academic Press. Granit, R., 1971. ‘The probable role of muscle spindles and tendon organs in eye movement control’. In: P. Bach-y-Rita and C.C. Collins (eds.), The control of eye movements. New York: Academic Press. Held, R., 1965. Plasticity in sensory-motor systems. Scientific American 213, 84-94. Helmholtz, H., 1867. Handbuch der physiologischen Optik. Leipzig: Voss. (Or see English trans. of 3rd ed., by later workers, by J.P.C. Southall, New York: Dover, 1962.) Hennessy, R.T. and H.W. Leibowitz, 1972. Laser optometer incorporating the Badal principle. Behavior Research Methods and Instrumentation 4, 237-239. Heuer, H., 1986. Perceptual aftereffects of sustained fixation and oculomotor changes. Paper presented at the conference on Sensorimotor Interactions in Space Perception and Action, University of Bielefeld, Febr. 1985. Acta Psychologica 63, 247-261 (this volume). Ivanoff, A. and C. Bourdy, 1954. Le comportement de la convergence en nocturne [The behavior of convergence in night vision.] Ann Optique Oculaire 3, 70-75. (Eng. trans available from DAO.) Leibowitz, H.W. and D. Moore, 1966. Role of changes in accommodation and convergence in the perception of size. Journal of the Optical Society of America 56, 1120-1123. Leibowitz, H.W. and D.A. Owens, 1978. New evidence for the intermediate position of relaxed accommodation. Documenta Ophthalmologica 46, 133-147. Leibowitz, H.W., R.B. Post and J. Sheehy, 1986. Efference, perceived movement, and illusory displacement. Paper presented at the conference ,on Sensotimotor Interactions in Space Perception and Action, University of Bielefeld, Febr. 1985. Acta Psychologica 63, 23-34 (this volume). Maddox, E.E., 1893. The clinical use of prisms: and the decentering of lenses, 2nd ed. Bristol: John Wright. Morgan, M.W., 1946. A new theory for the control of accommodation. American Journal of Optometry 23, 99-110. Morgan, M.W., 1968. Accommodation and vergence. American Journal of Optometry 45,415-454. National Academy of Science, 1983. Video displays, work, and vision. Washington, DC: National Academy Press. Owens, D.A., 1984. The resting state of the eyes. American Scientist 72, 378-387. Owens, D.A., in press. ‘Oculomotor information and perception of three-dimensional space’. In: H. Heuer and A.F. Sanders (eds.), Perspectives on perception and action. Hillsdale, NJ: Erlbaum.
D.A. Owens / Oculomotor tonus and visuul uduptation
231
Owens, D.A. and H.W. Leibowitz, 1976. Oculomotor adj,ustments in darkness and the specific distance tendency. Perception and Psychophysics 20, 2-9. Owens, D.A. and H.W. Leibowitz, 1980. Accommodation, convergence, and distance perception in low illumination. American Journal of Optometry and Physiological Optics 57, 540-550. Owens, D.A. and H.W. Leibowitz, 1983. ‘Perceptual and motor consequences of tonic vergence’. In: C. Schor and K. Ciuffreda (eds.), Vergence eye movements: basic and clinical aspects. Boston, MA: Butterworths. Owens, D.A. and K.S. Wolf, 1983. Accommodation, binocular vergence, and visual fatigue. Investigative Ophthalmology & Visual Science (Suppl.) 24, 23. Post, R.B. and H.W. Leibowitz, 1982. The effect of convergence on the vestibule-ocular reflex and implications for perceived movement. Vision Research 22, 461-465. Ramazinni, B., 1713. Diseases of workers. Eng. trans. by W.C. Wright. Chicago, IL: University of Chicago, 1940. pp. 323-325, 415-419. Schober, H., 1954. Uber die Akkommodationsruhelage. Optik 6, 282-290. (Eng. trans. available from DAO.) Steinbach, M.J., 1986. Inflow as a long-term calibrator of eye position in humans. Acta Psychologica 63,297-306 (this volume). Based on’Behaviora1 and anatomical evidence for eye muscle proprioception in surgically-treated humans. Paper presented at the conference on Sensorimotor Interactions in Space Perception and Action, University of Bielefeld, Febr. 1985. Swenson,H.A., 1932. The relative influence of accommodation and convergence in the judgement of distance. Journal of General Psychology, 7, 360-379. Turvey, M.T. and C. Carello, 1986. The ecological approach to perceiving-acting: a pictorial essay. Acta Psychologica 63, 133-155 (this volume). Based on Optical basis of controlled collisions. Paper presented at the conference on Sensorimotor Interactions in Space Perception and Action, University of Bielefeld, Febr. 1985. Von Hofsten, C., 1976. The role of convergence in visual space perception. Vision Research 16, 193-198. Von Hofsten, C., 1979. Recalibration of the convergence system. Perception 8, 37-42. Von Holst, E., 1954. Relations between the central nervous system and the peripheral organs. British Journal of Animal Behaviour 2, 89-94. Wallach, H. and K.J. Frey, 1972. Adaptation in distance perception based on oculomotor cues. Perception & Psychophysics 11, 77-83. Wallach, H. and P. Halpern, 1977. Eye muscle potentiation does not account for adaptation in distance perception based on oculomotor cues. Perception & Psychophysics 22, 427-430. Wallach, H., K.J. Frey and K.A. Bode, 1972. The nature of adaptation in distance perception based on oculomotor cues. Perception and Psychophysics 11, 110-16. Welch, R.B., 1978. Perceptual modification: adapting to altered sensory environments. New York: Academic Press. Wundt, W., 1862. Beitrlge zur Theorie der Sinneswahrnehmung. Heidelberg: CF. Winter’sche Verlagshandlung.