Perception, 1978, volume 7, pages 359-362

Sir Charles Bell on visual direction

Nicholas J Wade Department of Psychology, University of Dundee, Dundee DD1 4HN, Scotland Received 23 August 1977, in revised form-20 October 1977

Abstract. Helmholtz is usually credited with demonstrating the relationship between the perception of visual direction and eye muscle activity: he said that directional judgements resulted from the effort of will involved in altering the position of the eyes. However, Bell reached the same conclusion many years earlier, primarily on the basis of experiments with afterimages: an afterimage appeared to move with voluntary movement of the eye, but it appeared stationary when the eye was moved passively. The visual direction of an object is not determined by visual stimulation alone, as it also involves information about the position of the eyes. The information about eye position could derive either from efferent impulses to the eye muscles (often called outflow) or from the afferent impulses (inflow) from the stretch receptors in them (see Howard and Templeton 1966; Matin 1972). This distinction is generally attributed to Helmholtz (1866, 1925), who described several demonstrations supporting an outflow theory 6f visual direction. First, moving one eye passively (by pressing it or pulling the eyelid with the fingers) while observing an object with both eyes produces double images, and passive-movement of a single, open eye results in the apparent motion of visible objects. Second, afterimages remain stationary when the eye is moved passively, but they appear to move when the eye is rotated by its own muscular contraction. Third, individuals with paralyzed eye muscles experience apparent motion with attempts to move the eye by using the paralyzed muscle (Helmholtz 1925, pp 244-245). It seems clear from Helmholtz's account that these observations were not new, but their sources are not cited. His conclusion was that "These phenomena prove conclusively that our judgements as to the direction of the visual axis are simply the result of the effort of will involved in trying to alter the adjustment of the eyes" (Helmholtz 1925, p 245). The purpose of this note is to draw attention to the earlier work by Sir Charles Bell on visual direction, in which he made observations and reached conclusions similar to those of Helmholtz. The occurrence of double images when one eye is moved passively relative to the other was known to Aristotle: "Accordingly, just as if a finger be inserted beneath the eyeball without being observed, one object will not only present two visual images, but will create an opinion of its being two objects" (Beare 1931, pp 461b462a). A more precise description was given later by Robert Smith: "If by squinting or depressing an eye with ones finger, the optick axes are not directed to the same point; in these cases objects appear double: and now it is plain that the pictures are not painted upon corresponding places of the retina" (Smith 1738, pp 46-47). Bell (1803) restated this observation, but without citing Smith's earlier description (1) . ^ This oversight on Bell's behalf has led some historians (e.g. Flugel 1933) to consider that Bell was the first to suggest the idea of corresponding points, although these were clearly defined by Smith (1738, p 46). With respect to the observation of double images both Smith and Bell gave clear presages of the law of equal innervation: "The habit of directing the optick axes to the point in view is so strong that it is very difficult to do otherwise; [continued over]

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However, it was with regard to the apparent movement of afterimages that Bell best illustrated the manner in which visual direction is specified. "There is an inseparable connection between the exercise of the sense of vision and the exercise of the voluntary muscles of the eye. When an object is seen we enjoy two senses; there is an impression upon the retina; but we receive also the idea of position or relation which it is not the office of the retina to give. It is by the consciousness of the degree of effort put upon the voluntary muscles, that we know the relative position of an object to ourselves. The relation existing between the office of the retina and of the voluntary muscles, may be illustrated in this manner. Let the eyes be fixed upon an illuminated object until the retina be fatigued, and in some measure exhausted by the image, then closing the eyes, the figure of the object will continue present to them: and it is quite clear that nothing can change the place of this impression on the retina. But notwithstanding that the impression on the retina cannot be changed, the idea thence arising may. For by an exertion of the voluntary muscles of the eye-ball, the body seen will appear to change its place, and it will, to our feeling, assume different positions according to the muscle which is exercised. If we raise the pupil, we shall see the body elevated, or if we depress the pupil, we shall see the body placed below us; and all this takes place while the eye-lids are shut, and when no new impression is conveyed to the retina (2) . The state of the retina is here associated with a consciousness of muscular exertion; and it shows that vision in its extended sense is a compound operation, the idea of position of an object having relation to the activity of the muscles. If we move the eye by the voluntary muscles, while the impression continues on the retina, we shall have the notion of place or relation raised in the mind; but if the motion of the eye-ball be produced by any other cause, by the involuntary muscles, or by pressure from without, we shall have no corresponding change of sensation." (Bell 1823a, pp 178-179) Bell also mentioned that forming a binocular afterimage and then pressing on one eye did not result in either movement or double images, contrary to the situation with real images. In addition he described the case of a patient with a totally paralyzed eye, but he did not comment on her visual functions other than to note that "the vision is entire" (see also Bell 1823b). [The results of paralyzed eye experiments have been reinterpreted recently by Matin (1976).] Bell summarized his endeavours thus: "These experiments and this explanation of the effect of the associated action of the voluntary muscles of the eye-ball, appear to me to remove an obscurity in which this subject has been left by the latest writers. In a most scientific account of the eye and optics, lately published, it is said on this question, "we know nothing more than that the mind residing, as it were, in every point of the retina, refers the impressions made upon it, at each point, to a direction [footnote (1) continued] insomuch that when one eye is shut and the other is in motion one may feel by ones fingers laid upon the eye-lid, that the eye which is shut, always follows the motions of the eye that is open" (Smith 1738, p 46). Bell elaborated upon this as he, too, found it impossible "to distort one eye inward or outward, and at the same time keep the other fixed" because "in making the eyes converge or diverge the will is acting upon both eyes equally" (Bell 1803, p 360). W These observations were made earlier by Darwin (1786), who was concerned to show that the movements of an afterimage were not due to movements of bodies in the aqueous humour. This was done by demonstrating that the afterimage in an eye maintaining steady fixation did not appear to move.

Sir Charles Bell on visual direction

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coinciding with the last portion of the ray which conveys the impress"" (Bell 1823a, p 180). The unnamed authority to whom Bell referred was Brewster (1821), who was not slow to pen a characteristically vitriolic reply. Brewster (1825) did not dispute Bell's observations, but made several others which were considered to invalidate Bell's conclusions. First, he found that an afterimage follows the motion of the head when this is turned by the neck alone, from which he argued that there was a relationship between the neck muscles and visual direction. He also reported that the rotation of the whole body on a stool resulted in equivalent motion of an afterimage. In both of these cases there would have been reflex compensatory eye movements due to stimulation of the vestibular system (see Hansen and Skavenski 1977; Howard and Templeton 1966). However, Brewster was only concerned with excluding the "consciousness of exerting the voluntary muscles of the eye-ball" (Brewster 1825, p 4). Bell should have been sympathetic to this criticism, because he had addressed himself earlier to the related problem of postrotational afterimage movement. It had been known since Darwin (1786) that afterimages appeared to move in the direction opposite to previous body rotation, and Bell (1803) described some experiments by Wells on this matter. Wells noted that an afterimage, generated before rotation, appeared to move after turning, even though his eyes felt stationary (3) . He then directed another person to repeat the experiment, and observed that after rotation the eyes did move. From these observations Bell (1803) concluded that the body rotation produced the involuntary movements of the eyes, which led to the postrotational afterimage movement. Nonetheless, he did not qualify his later statements with regard to the dependence of visual direction on the consciousness of the effort put into moving the eyes (Bell 1823a) in the light of these earlier reflections. Why have Bell's observations not been incorporated into the literature on visual direction? One possibility concerns the importance placed upon Johannes Muller's (1826a) monograph and his handbook (Muller 1839, 1842) by subsequent writers. [Helmholtz cited Muller (1826a) when considering visual direction, and Boring (1942) commenced his discussion of eye movements with this book.] Muller considered that afterimages moved in the same manner as the eye under all conditions. Indeed, he used this to distinguish between afterimages and imaginary images ("die phantastischen Bilder"), which remained stationary during eye movements (Muller 1826b). However, his later discussion of visual direction (Muller 1842) was in terms of the optical projection alone, and no reference was made to Bell (4) . Eye movements were mentioned with respect to visual motion perception: "We judge the motion of an object, partly from the motion of its image over the surface of the retina, and partly from the motion of our eyes following it" (Muller 1842, p 1178). With regard to the latter he mentioned the alternatives of judging motion on the basis of impulses from the eye muscles, or from impulses sent to them. However, he failed to distinguish between these experimentally, in the manner that Bell (1823a) had done using afterimages. (3) Porterfleld (1759) described the apparent rotation of objects in the direction opposite to previous body turning, but he stated, mistakenly, that the eyes remained absolutely at rest following rotation. (4) Moreover, Bell is not mentioned in Muller's discussion of identical retinal points (Muller 1826a, 1842), nor with regard to the doctrine of specific nerve energies, which had been outlined by Bell (1811, 1823b). Muller appears to have relied more heavily on Magendie's writings than on Bell's on the issue of priority concerning the functions of the dorsal and ventral spinal nerve roots: Muller stated, incorrectly, that Bell did not provide any experimental evidence in support of his idea. This error was corrected in a footnote by Baly in his translation (see Muller 1839, p 690). Muller's reliance on Magendie was unlikely to have led to an objective appraisal of Bell's work (see Carmichael 1926).

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N J Wade

Thus, it appears that Sir Charles Bell should be credited with demonstrating the relationship between the perception of visual direction and eye muscle activity. Acknowledgements. This research was supported by a grant from the Medical Research Council. I am grateful to John Findlay for commenting on an earlier draft of this paper. References Beare J I, 1931 Parva Naturalia. De Somniis in The Works of Aristotle Translated into English volume III Ed. W D Ross (London: Oxford University Press) pp 461b-462a Bell C, 1803 The Anatomy of the Human Body volume III (London: Longman, Rees, Cadell and Davies) Bell C, 1811 Idea of a New Anatomy of the Brain reprinted in Gordon-Taylor Sir G, Walls E W, 1958 Sir Charles Bell. His Life and Times (Edinburgh: Livingstone) pp 218-231 Bell C, 1823a "On the motions of the eye, in illustration of the uses of the muscles and of the orbit" Philosophical Transactions of the Royal Society 113 166-186 Bell C, 1823b "Second part of the paper on the nerves of the orbit" Philosophical Transactions of the Royal Society 113 289 - 307 Boring E G, 1942 Sensation and Perception in the History of Experimental Psychology (New York: Appleton-Century-Crofts) Brewster D, 1821 "Optics" Edinburgh Encyclopaedia volume XV (Edinburgh: Blackwood) Brewster D, 1825 "Observations on the vision of impressions on the retina, in reference to certain supposed discoveries respecting vision announced by Mr. Charles Bell" Edinburgh Journal of Science 2 1-9 Carmichael L, 1926 "Sir Charles Bell: a contribution to the history of physiological psychology" Psychological Review 33 188-217 Darwin R W, 1786 "New experiments on the ocular spectra of light and colours" Philosophical Transactions of the Royal Society 76 313-348 Flugel J C, 1933 A Hundred Years of Psychology 1833-1933 (London: Duckworth) Hansen R M, Skavenski A A, 1977 "Accuracy of eye position information for motor control" Vision Research 17 919-926 Helmholtz H, 1866 Handbuch der Physiologischen Optik Dritter Band (Leipzig: Voss) Helmholtz H, 1925 Physiological Optics volume III, English translation by J P C Southall for The Optical Society of America (Menasha, Wis.: Banta) Howard I P, Templeton W B, 1966 Human Spatial Orientation (Chichester, Sussex: John Wiley) Matin L, 1972 "Eye movements and perceived visual direction" in Handbook of Sensory Physiology volume VII/4 Visual Psychophysics Eds D Jameson, L M Hurvich (Berlin: Springer) pp 331-380 Matin L, 1976 "A possible hybrid mechanism for modification of visual direction associated with eye movements—the paralyzed-eye experiment reconsidered" Perception 5 233-239 Muller J, 1826a Zur vergleichenden Physiologie des Gesichtssinnes des Menschen und der Thiere, nebst einen Versuch fiber die Bewegungen der Augen und iiber den menschlichen Blick (Leipzig: Cnobloch) Muller J, 1826b Uber die phantastischen Gesichtserscheinungen (Coblenz: Holscher), reprinted in Ebbecke U, 1951 Johannes Muller der grosse rheinsche Physiologe (Hannover: Schmorl and von Seefeld) Muller J, 1839 Elements of Physiology volume I, English translation by W Baly (London: Taylor and Walton) Muller J, 1842 Elements of Physiology volume II, English translation by W Baly (London: Taylor and Walton) Porterfleld W, 1159 A Treatise on the Eye, the Manner and Phaenomena of Vision (Edinburgh: Hamilton and Balfour) Smith R, 1738 A Compleat System of Opticks in Four Books (Cambridge: published by the author)

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Sir Charles Bell on visual direction.

Perception, 1978, volume 7, pages 359-362 Sir Charles Bell on visual direction Nicholas J Wade Department of Psychology, University of Dundee, Dunde...
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