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The monocular eye movements of the pigeon
Vision
Ru.
Vol.
9. pp.
133-144.
THE
Pergamon
Press 1969.
Printed
MONOCULAR OF THE
in
Gr~l Britain.
EYE MOVEMENTS PIGEON1
PATRICK W. NYE Division of Applied Science, California Institute of Technology, Pasadena (Received 29 July 1968; in revised form 24 September 1968) INTRODUCTION
HEADmotion undoubtedly serves an important functional role in the visual and kinesthetic organization of the pigeon’s nervous system and it has received attention in a number of studies. DUNLAP and MOWRER (1930) showed that nictitation occurred during practically all the thrusting movements which are characteristically made during walking. Later BUYS and RIJLANT (1932) and MOWRER (1935) examined the vestibular head nystagmus in response to angular acceleration and VISSERand RADEMAKER (1934) described both the vestibular and the optokinetic head nystagmus and showed that the phenomenon remained essentially unaffected after decerebration. However, head motion is probably not the only aspect of the visual-kinesthetic response. Nevertheless, throughout all these studies, the question whether eye movements within the head make any significant contribution to the overall function of the oculomotor system was apparently overlooked. This may have been due to the fact, which is easily demonstrated by a pigeon held in the hand, that the head is sufficiently mobile to provide 360 deg visibility of its surroundings without recourse to eye movement. Thus it was possibly assumed that eye movement was unnecessary and therefore absent or unimportant. Before going on to examine the nature and role of pigeon eye movement it will be worthwhile at this point to give some detailed consideration to the structure of the pigeon eye and orbit. Of the three main types of avian eye, the globose, the tubular and the flat, the last named is found to be common to the largest proportion of birds. The pigeon possesses the flat type of eye which is encased in a tightly fitting socket and is controlled by a system of thin ribbon-like muscles. CHARD and GUNDLACH (1938) have estimated in the horizontal plane that the total field of vision of the pigeon eye is in the region of 172 deg and that the bird has a binocular visual field of about 24 deg. Thus using both eyes, visibility can be achieved over an angle of almost 300 deg. Moreover, studies of the receptor distribution in the retina have shown that the pigeon possesses a uniform densely populated mascula-like area capable of providing good acuity over a visual angle considerably in excess of the l-5-2.0 deg characteristic of the human fovea. Taking all these facts into account, the authors have concluded that eye movements must be of little importance in extending the visual field. It therefore appears that both the mobility of the head and the geometry of the eyes obviate the necessity for large eye movement; nevertheless, it is probable that some eye 1This research was supported by the National Institutes of Health USPHS Grant NE 03627. 133
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PATRICK w.
NYE
movement is required for the important function of maint~n~g acuity. Numerous studies of human observers by D~TCH~URNand CISSBORG (19.52), Rr~cs et al. (1953), D~~CHBURNet al. (1959), BARLOW(1963) and many others have demonstrated that small involuntary eye movements serve to sustain good acuity by ensuring that the retinal receptors receive a constantly fluctuating stimulus along contours and boundaries in a pattern and are not permitted to suffer the adaptation effects which occur with stationary or near stationary retinal images. The involuntary eye movements of a normal fixating human subject are bounded within an area of diameter 30 min arc and are not usually visible to the naked eye of an observer. However, despite the fact that the pigeon would ostensibIy appear to have Iittle use for large eye rotation, it can usually be seen by relatively casual observation to make very active eye movements. This fact has been noted by a number of authors, among them WALLS(1942) and POLYAK(1957). In addition, MATURAXA(1962) observed that decerebrate pigeon preparations make rapid oscillatory bursts of eye movement at periodic intervals, but, in view of the acute condition of the animal, it was not certain whether these oscillations had any relationship to the eye movements of a normal bird. It is possible to hypothesize that, to a first approximation, head motion in the pigeon serves the same purpose as does the large voluntary eye movement of the human observer whilst small oscillations of the eyeball in its socket may be present which correspond to the involuntary physiological nystagmus of the human eye. FoIlowing a recent study of the binocular visual acuity of the pigeon (NYE, 1968) some observations on eye movement were made to examine this hypothesis and to indicate the degree to which the possible presence of a physioIo~ca~ nystagmus could infiuence the contrast threshold for a repetitive pattern. The present paper reports some measurements which have been made upon the monocular eye movements of intact partially anaesthetized pigeons and of normal pigeons. METHOD The movements of the eye were recorded by means of a beam of light reflected from a mirror attached directly to the eye. Mirror attachments were made to the left eye at the posterior rim of the cornea with the mirror center located on the horizontal meridian. Each mirror was a 4-5 mm2 aluminized chip cut from a No. 1 microscopeslide and WeiotKd about 4 mg. A powder type of denture adhesive (Corega Chemical Co.) was used to secure the mirror firmly. Figure 1 shows the design of the optical system. Light from a point source S & transmitted by the Iens Lt to form a collimated beam which iUuminates the horizontal and vertical sIIt aper&ues of the target at T. In its turn T is situated at the focus of a lens La which forms an image of S on the mirror Mt attached to the eye. Upon refiection from Mt the beam is directed by the beam splitter B through the iens L3 which formf an image of T in the pIane of a pair of triangtdar apertures placed at A. The light passing through the two sections of the mask is routed to two sqmte phot~rn~tip~ tubes (PMH and PMv) which am positioned with their cathodes in conjugate image planes, formed by the lens I.+ with respect to the mirror Ml. Crosschannel rejection (between the horizontal and vertical channels) to better than 40 db was achieved by the introduction of polarizers at T with their axes of polarization aligned with the individual slits: analysers PH and Pv were orientated perpendicularly in such a way as to block the unwanted signals. The total available field of the optical -tern was about 7.5 deg. Signals from the photo-multiplier tubes were amplified, sampled, converted into digital form and recorded on magnetic tape together with the calibration curves required to convert to angular measure. The intrinsic noise Ievel of the overail system was 12 YX arc (RMS) for the horizontal channel and 8 see arc (RMS) for the vertical channel. The tracings of eye position were obtained by means of a simple computer algorithm. The pigeons were securely held by the head with a beak clamp and ear bars, foilowing the usuat stereotaxic procedure, and orientated with respect to the horizontal and vertical axes of the optica system as shown in Figs. 1 and 2. In ail but a few experiments the p&eons were initially anaesthetized with HaIothane and, for convenience; stied in that condition untif the head had been secured, the mirror Mi attached to the eye and the bird positioned correctIy in the apparatus. Apptiitioo of the anaesthetic was then discontinued and the bird aifowed to recover whilst eye movement recordings were
The Monocular Eye Movements of the Pigeon
135
A ?MV h TO COMP!J TE?
FIG. 1. Above: Schematic diagram showing the position of the bird in relation to the principal axes of the optical system. Below: Rectangles T and A illustrate the target apertures at T with Polaroid filters attached and the triangular apertures at A on which the image of T is formed (see text). being made. In all cases a local anaesthetic was applied to the ears and a 10 per cent cocaine solution applied to the left eye. Also, to prevent blinking movements from dislodging the mirror, the nictitating membrane was removed several weeks prior to the experiments and the upper and lower lids were held apart by retractors. Approximately half of the pigeon’s left, horizontal visual field was obscured by the apparatus whilst the binocular and a portion of the lateral visual field remained unhindered. A total of six birds were examined in the eye movement apparatus. VERTICAL AXIS
i
HORIZONTAL \
AXIS
F
SUPPORT
FIG. 2. The position
of the head relative to the horizontal
and vertical axes of measurement.
136
PATRICK
W. Nn
RESULTS
A representative example of eye movement sampled at a rate of 250 per set and recorded whilst under partial anaesthesia is shown in the upper half of Fig. 3. Short
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Fro. 3. Above: Horizontal (Ii) and vertical (V) components of the eye movement of a partMy amuathetkgi &eon. +&w: Eye moveymnt fron? the same bird following recovery anac&wa. Note unpuhe in lower r&t-hand comer.
bursts of oscillation at a frequency of 27 Hz and peak to peak amplitude of l-5 deg occur at intervals of about l-3 set with the addition of some occasional impulsive movements. One of these impulses is shown following the second oscillatory burst in Fig. 3. The lower half of Fig. 3 shows a record taken from the same bird about 15 min later when it had fully recovered. The osciliatory bursts have substantially increased in amplitude reaching a peak to peak level of 5 deg when resolved in the vertical direction. A vertical impulse whose amplitude exceeds 1.6 deg is shown in the lower right-hand corner of Fig. 3 and is of interest for the fact that, although it indicates a movement whose velocity is comparable with that found during oscillatory motion, there is nevertheless no subsequent oscihation. The nature of this movement is therefore different and it is seemingly made under the restraint of an overdamped control system. Apparent tracking eye movements were also observed but only during the uide awake phases of experimental sessions. These were slow drift movements of eye position from one fixation point to the next at a rate of approximately l-5 deg/sec with total excursions in the region of 3-5 deg but sometimes exceeding the maximum range of the recording system (7.5 deg). Figure 4 shows the response to a small light source moving in the horizontal plane. Whilst it cannot be said that the precision is high there is more than a suggestion that the eye is following the target. Active eye movement of this type would occur reliably only if the target motion was irregular. Periodic motion to and fro would commonly lead to a rapid loss of interest which could be rearoused by a sudden change or cessation of the target motion. Bearing in mind the fact that the head was immobile, the data indicated that there are some ocuiomotor functions which can be
The Monocular
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Eye Movements of the Pigeon
k
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TIME (SECONDS)
FIG.4. Eye movements
made by a pigeon in response to a self luminous target 8 mm in diameter moving in the anterior visual field at a distance of 30 cm from the eye. Target motion is indicated by the lowermost trace and a downward deflection represents movement
in the posterior direction. expressed by eye movement although they may not operate in quite this way in the normal bird. It is, however, certain that the eye can respond more rapidly than the head and it was in response to a rapid change in the target that a pattern of movement closely resembling the flick, observed frequently in human eye movement, wouId occasionally occur. A flick, which is a rapid change of fixation taking place in less than 20 msec, can be seen in the upper left-hand corner of Fig. 4. However, the frequency of occurrence of these movements was very low, an observation which contrasts sharply with what is known of human eye movement under similar conditions (DITCHBURN and FOLEY-FISHER, 1967). Moreover, unlike that of the human observer, the pigeon eye appears to have very little physiologica tremor for it was not possible to detect it above the intrinsic noise level of the measuring system. The recording of an oscillatory movement shown in Fig. 5 was sampled at a rate 5HORIZONTAL
Y
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FIG.5. An oscillatory burst of eye movement shown against an expanded time scale.
of 2500 per set and shows the structure of the oscillatory wave form in more detail. The burst of oscillation itself was used to trigger the sampling process, and the section of the record preceding the crossing of the trigger threshold has inevitably been omitted. In Fig. 6 the horizontal and vertical waveforms of Fig. 5 have been plotted
138
w. NYE
P.MRICK
ANTERIZR
POSTERIOR !
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FIG. 6. A plot, in angular space, of the motion shown in Fig. 5. Approximate of the principal eye muscles are also indicated.
positions
against each other to give a trace of eye position in angular space. Surrounding this plot is a plan of the approximate directions of action of the principal eye muscles. The motion of the eye is seen in this case to be an elliptical spiral. In each of five pigeons examined, the trajectories have all been roughly elliptical (although not always describing as well defined a spiral as chat shown) and with their major axes rotated from 20430 deg anti-clockwise from the horizontal meridian. The frequency of the oscillation was found to range from 28-35 Hz and to be sustained for periods of up to O-8 sec. Starting points and terminal fixation points for an oscillation were seldom the same except when under partial anaesthesia. Usually the visual axis would either drift back, over a period of l-2 set, to the position originally occupied or remain at the new fixation point. The form of the decaying oscillation initially suggests the idea that it is the impulse response of an inertial load suspended from a system of passive underdamped elastic muscles. However, this appears to be an over simplification. In fact there is some evidence which indicates that much of the response is under voluntary control. Firstly, as shown in Fig. 7, occasional pulses are observed in which the oscillation is interrupted
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FIG. 7. A typical interrupted oscillatory movement which illustrates that the eye motion is not a ringing response to a single impulse but apparently under continuous control.
The Monocular Eye Movements of the Pigeon
139
for a period of about O-1 set and then continues. Secondly. it is found that the rate of decay can fluctuate from pulse to pulse and also within a single pulse. Finally, some pulses begin with relatively small excursions, climb rapidly in amplitude within two or three cycles and decay slowly over the course of a further ten cycIes. This is not the type of behavior to be expected from a passive mechanical system which has fixed parameters. To achieve such a response, either the damping applied must be controlled and vary widely from large values in the case of an impulse movement or flick to a range of underdamped values during the oscillatory pulses or, the eye muscles must be capable of exerting a flexible variety of force patterns upon a permanently overdamped system. It is convenient for the purpose of discussion to summarize these observations under a list of categories some of which were originally adopted to describe human eye movements (DITCH~URNand GINSBORG, 1953) but the use of these categories should not be taken to imply that the eye movements are identical in the two cases. Flicks are observed in fully conscious alert pigeons particularly when responding to target motion. However, the frequency of flicks relative to similar events in human eye movements is extremely low and it is possible that in an unrestrained bird this visual function is served to some extent by head motion. Impulse movements occur more frequently than flicks. Their amplitudes range up to 2 deg. Nevertheless they do not stimulate oscillatory activity and are therefore under a different mode of control. Drifts occur when there are objects moving in the visual field. They commonly take the form of movements between fixation points with velocities of about l-5 deg per sec. Tremor is not visible above the intrinsic noise level of the recording system and must lie below 12 set arc (RIMS). Oscifluhzs of the pigeon eye occur in short bursts at rates of about 30 Hz and with amplitudes of severat degrees. There is evidence that indicates that this motion is under active control and the rate of the oscillation is all the more remarkabIe when it is recalled that the maximum frequency at which human eye movements of comparable amplitude can be made is no more than 2 Hz (FENDERand NYE, 1961). DISCIJSSION
A considerable body of data on the involuntary eye movements of human subjects and their role in maintaining long term acuity has been gathered in recent years. It has been shown by DITCHBURNet al. (1959) that the eye movements which provide the most effective stimuli to the human visual system are rapid saccadic deflections of the visual axis called flicks. Studies of the fine tremor motion, which is also present, suggest that this component, summed over all frequencies, couId contribute to the m~ntenan~e of acuity although the evidence is not strong and the effect likely to be small. Setting aside the gross rotational movements, one could have reasonably expected that some saccadic eye movement would be found in the pigeon because it may be assumed that the mechanisms in the human eye which adapt to stationary retinal images also exist in the eyes of other vertebrates. However, the variety and scale of the pigeon eye movement is so different from that found in the human that it is difficult to interpret the function of its various components in quite the same terms. Much of the eye motion which can be said to resemble human involuntary eye movement is carried out voluntarily by the pigeon when stimulated by some moving object. Thus the fact that flicks have been found to occur relatively rarely, probably reflects the limited interest which the experiment holds for most pigeons rather than the degree of activity to be expected from an unrestricted bird.
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PATRICKw. NYFi
Impulsive movements are much more common. They range up to 2 deg in amplitude and also appear more numerous under conditions of visual stimulation. In partially anaesthetized birds impulse movements were observed at intervals of about 30 set and increased in frequency, with progress toward recovery, to rates of approximately one in 5 sec. Comment on the origin of this component will be postpdned to later in the discussion. Efforts to identify significant tremor motion have not been successful and this component, which must exist at some level, lies below the intrinsic noise of the recording system. ‘IX implies that the amplitude is less than the intercone spacing for fovea1 vision (about 30 set arc). Moreover, on the basis of the data reported by DWHBURN et al. (1959), such small movements would be totally ineffmtive in stimulating the visual system of a human observer and p~sumab~y this is also true for the pigeon. An explanation of the origin and purpose of the oscillatory movements is required at this point and several questions come naturally in the following order. The first questions are concerned with artifacts. Is the motion a peculiar consequence of unusual stimulus conditions or of physiological stress generated by the experimental procedure? Two of the most important questions in this vein have been examined. The first concerns the possibility that the motion is brought about by scattered light, casting onto the retina a shadow of the edge of the mirror attachment, in such a way that the loop gain of the visual feedback obtained when tracking this stimulus is increased. This could cause the ocuiomotor system to enter a region of instability (FENDERand NE, 1961) giving rise to the oscillation. However, observations made with infra-red light have shown the response to be unchanged. Another possible source of artifact is that the pressure exerted by the stereo&& ear bars might create a disturbance of the v~tibu~ar system and thus generate a form of nystagmus. Nevertheless, it has also been possibte to dispose of this speculation by reference to the results of experiments performed upon two cooperative unanaesthetized pigeons restrained only at the wings and legs and allowing free movement of the head. Several oscillatory bursts were recorded together with most of the salient features previously described, hence, vestibular interference is not involved and the conclusion must be drawn that the oscillations are a part of a normal behavioral pattern. The next questions revolve around whether the motion is directly related to an act of visual discrimination or merely serves some peripheral function. Attending to the first point, it is clearly difIicult to reconcile such farge and rapid movements with purposeful visual scanning although there is evidence which suggests that they are under some degree of control. On refiection, therefore, it appears more likely that the osciitation has an indirect function related to the act of blinking and this conclusion is supported by the following additional data. The use of a topical anaesthetic and eye lid retractors during the recording of eye movements destroys the opportunity to observe the timing of blinks directly and the restraint placed upon head movement makes it impossible to determine precisely where the oscillatory eye movements fit into an overall activity pattern. In an effort to overcome some of these difficulties and obtain observations in conditions more closely resembling the normal state, bipolar electrodes made from 0*076 mm dia. teflon-coated platinum iridium wire were inserted into the orbits of the Ieft eyes of two pigeons in the region of the superior oblique and rectus muscles. Electrode leads were then attached to a strip connector (Microdot) fixed onto the skuf! with size O-80 x 0.125 in. stainless
141
The Monocuiar Eye Movements of the Pigeon
steel bolts and Caulk grip cement. Simultaneous recordings of eye movements and muscle potential signals were then made. A short segment of a recording is shown in Fig. 8(a). Oscillatory bursts were always accompanied by sustained muscle activity
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FIG. 8(a).
The upper three traces were recorded simultaneously and show the horizontal and vertical components of eye movement (scale shown at left) together with the corresponding muscle potentials (Mf obtained from electrodes inserted into the orbit. (b). The lower pair of traces have been selected from simultaneous recordings of the eye muscle potentials and a time of event switch (B) attached to the upper eye lid.
whilst impulsive movements were associated with substantially shorter periods of muscle action. In a supplementary group of experiments a switch was constructed from O-1 mm dia. tinned copper wire and attached to the left eye lid of an unresir~ned bird in such a way that a blink closed the contact and provided a time of event signal with very little hinderance to eye lid performance. From further recordings of eye muscle potentials made whilst walking and feeding it was an easy matter to identify the sustained muscle activity which indicated oscillatory eye movements. Figure 8(b) shows a pattern which was repeatedly demonstrated, namely that each sustained burst of muscle activity was precisely correlated with a blink. Shorter bursts of muscle activity presumably associated with impulse movements were also often accompanied by blinks but the correlation was not high, possibly because the switch failed to respond to short high speed motion. Thus the results showed that some impulse movements and a substantial proportion, if not all, of the oscillatory activity normally occurs during a blink. The most commonly accepted function of the blink reflex is that given by SLONAKER (1918), namely, that the nictitating membrane keeps the cornea free from dust and other foreign matter. It would therefore seem probable that the purpose of the eye motion is to provide a polishing action between the cornea and the papiliary lining of the nictitating
hITUCK W. NYFi
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membrane. However, there is another possible functiou of nictitation which has been suggested by DUNLAP and MOWRER (1930). They observed a close correlation between nictitation and head movement and concluded that the membrane may blank out or suppress vision during the motion and hence sustain the percept of world stability. In view of this proposal it is interesting to note that in Fig. 8(b) and elsewhere, the period of a blink is almost always shorter than the period of the corresponding muscle action and it is apparent that the eye is still in rapid motion when the blink has been completed and the eye fully opened. Whether this is a normal behavioral response, or represents a lack of coor~nation which disappears when the animal is in more congenial surroundings, is difficult to determine; but if the data do indicate the true sequence of events the oscillating visual image could be highly confusing unless centrally compensated by precise proprioceptive or motor outflow information. Either one or both sources of information could be available but in their absence it is conceivable, as suggested by RICHARDS(1968), that a degree of suppression couid result from a depoiarisation of the retina caused by the action of shearing forces between the retina and the vitreous generated during the oscillation. It is apparent from this discussion that the evidence as a whole points to the conclusion that the oscillatory component has no direct role in visual discrimination and indicates that although the rotational range of the pigeon eye is smaller than our own, it possesses, in contrast to what is often assumed, a well developed oculomotor system capable of generating a repertoir of eye motion which in some respects exceeds our own in speed and agility. Moreover, one final remark should be added, namely, that from the practical viewpoint of the electrophysiologist working on the visual system of an acute pigeon preparation it is clear that the risk of artifact arising from such large eye movements as those reported here is very high and the mobility of the eye can no longer be ignored or its immobility tacitly assumed. REFERENCES
B. (1963). Slippage of contact lenses and other artifacts in relation to fading and regeneration of supposedly stable retinal images. Q. Jl exp. PsychoA l&36-51. Buvs, E. and RLfLANT,P. (1932). Mkthode d’exploration de l’oreille interne non acoustique. Compt. rend. SIX. Biei. 110,986-988. CHARD,R. D. and GUNDLACH,R. H. (1938). The structure of the eye of the homing pigeon. J. camp. BARLOW,H.
Psych& 25, 249-272. DITCHBURN,R. W.
and GINSBORG,B. L. (1952). Vision with a stabilized retinal image. Nuture, Lond.
170,36-37.
DITCHBU~N,R. W., FENDER,D. I-i. and MAYNE, S. (1959). Vision with controlled movements of the retinal image. J. Physiot. 14!5,9&107. DXTCHBURN,R. W. and FOLEY-FISHER, J. A. (1967). Assembled data in eye movements. Uptica Acta 14, 113-l IS. DUNLAP, K.
and Mowaaa, 0. H. (1930). Head movements and eye functions of birds. J. cotnp. Psychol. 12, 99-l 12. FENDER,D. H. and Nn, P. W. (1961). An instigation of the mechanisms of eye movement control. Kybernettk 1, 81-88.
MA-A, H. R (1962). Functional organization of the pigeon retina. In: Information Processing in the Nervous System. (Proc. XXII International Congress, Leiden, 1960) pp. 170-178. Movvaazt, 0. H. (1935). The nystagmic response of the pigeon to constant angular acceleration at Iiminal and supmliminal intensities. J. camp. Psychol. 19, 177-193. NYE, P. W. (1968). The binocular acuity of the pigeon measured in terms of the modulation transfer function. vision Res. 8, 1@41-1053. PoLYAK,S. L. (1957). 27zeVertebrate Visual System. Univ. of Chicago Press, Blinois. RICHARDS, W. A. (1968). Visual suppression during passive eye movement. J. opt. Sot. Am. 58,1159-l 160.
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RIGGS, L. A., RATLEF, F., CORNSWEET, I.D. and CORNSWEET, T. N. (1953). The disappearance of steadily fixated visual test objects. 3. opt. Sot. Am. 43, 495-501. SLONAKER, J. R. (1918). A physiological study of the anatomy of the eye and its accessory parts of the English sparrow. J. Morphol. 31, 351450. VISSER,J. and WEMAKER, G. G. J. (1934). Die optischen reaktionen grosshimloser tauben. Mitteilung I. Archs N
Abstract-The monocular eye movements of both restrained and partially restrained pigeons have been measured by means of a mirror attached to the edge of the cornea. The principal observations may be summarized under the following categories. Flicks, or eye movements which bring about a rapid change of fixation, are found to occur only in response to sudden and unexpected motion of a visual stimulus and are rarely observed under the quiescent conditions of a darkened room. Drips, which are slower movements of the eye between fixation points, occur at velocities of about l-5 deg per set and are stimulated by object motion. Tremor motion is of extremely low amplitude and is unlikely to serve any visual function. Oscillarions occur in short bursts at frequencies of about 30 Hz and amplitudes of several degrees. The evidence indicates that this eye movement is normally executed during a blink and it is probable that it performs a polishing action on the cornea in conjunction with the nictitating membrane. The observations lead to the conclusion that although the range of rotational motion available to the pigeon is less than in man, it nevertheless possesses a well developed and precisely controlled oculomotor system which appears in some respects to out-perform our own. Resume-On mesure les mouvements monoculaires des yeux du pigeon par un miroir fise au bord de la comee. On peut resumer les principales observations sous les categories suivantes. Mouvements rapides de changement du point de fixation, ne se produisant qu’en reponse a un mouvement soudain et inattendu du stimulus visuel, et rarement observes dans le calme dune chambre sombre. DPrives, mouvements plus lents de l’oeil entre des points de fixation, avec des vitesses de 1 A 5’ par set et stimults par le mouvement de l’objet. Tremblement de t&s faible amplitude, probablement sans fonction visuelle. Oscillations, par bouffees courtes ;i des frequences voisines de 30 Hz et des amplitudes de quelques degrts. 11 semble que ce mouvement de l’oeil se produise normalement pendant un clignement et serve probablement a polir la comee, en conjonction avec la membrane nictitante. De ces observations on conclut que, quoique le domaine de rotations possibles soit moindre pour le pigeon que pour I’hornme, il posstde cependant un systtme oculomoteur bien developpe et control6 avec precision, systtme qui g certains points de vue semble surclasser le notre. Zusammenfassung-Die monokularen Augenbewegungen sowohl von hxierten als such von teilweise ftxierten Tauben wurden mit Hilfe eines Spiegels gemessen, der am Rande der Hornhaut befestigt war. Die hauptsichlichen Beobachhmgen konnen in folgenden Kategorien zusarnrnengefal3t werden. Flicks oder Augenbewegungen, die eine schnelle Verlnderung der Fixation bewirken, wurden nur als Reaktion auf eine schnelle, unerwartete Bewegung eines visuellen Reizes gefunden und werden selten unter den ruhigen Bedingungen eines verdunkelten Raumes beobachtet. Drifbewegungen, das sind langsamere Augenbewegungen zwischen den Fixationspunkten, die mit einer Geschwindigkeit von ungefahr l-5 Grad pro Sekunde auftreten, werden von der Objektbewegung hervorgerufen. Zitter-Bewegungen weisen eine garu besonders niedrige Amplitude auf, und es ist unwahrscheinlich, daB sie irgend einer visuellen Fur&ion dienen. Schwingungen treten in kurzen Ausbriichen mit Frequenzen von ungeflhr 30 Hz und Amplituden von mehreren Grad auf. Der Augenschein zeigt, da0 diese Bewegung norrnalerweise w&rend eines Lids&lags ausgefiihrt wird, und es ist wahrscheinlich, daB sie, zusammen mit der Nickhaut, eine polierende Wirkung auf der Homhaut bewirkt.
144
PATRICKW.NYE Die Beobachtungen fdhreo zu dem Schlul3, da0 obwohl der Bereich van Drehbeweguogeo, der der Taube zu@o&ich ist, geringer als beim Meoscheo ist, sie trotzdem ein guteotwickeltes uod p&se koatrolliertes okulomotoriscks System beaitzt, welches in mancher Hiosicht dem unseren iiberlegen ist. MoHoKynrrpHbte Awsxcetw~ mxia rony6e& nonmmbK) RUIN PRO 6bl~~~~net10~a~~cno~ont6~)3epKana,npwpennemroro~~pa~, pOrOBHIXbI. ~HOBHbIe pe3yJIbTaTbI HaBnwAeH@ MOW 6bmb cy%fMHpOeaWr UIeAyIORIHMO6pa3OM: cKf?‘fKU mm mmemm rna3, KOTOPffe ~P-A~T K 6bnpot cMeHe &DxaKHE H B03HHKalOT TOJIbKO B OTBCT Ha &W3KOC Ef HCO~NIHoe JWUKCEHC 3pEfRJIbHOrO
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Ru.
Vol.
9. pp.
133-144.
THE
Pergamon
Press 1969.
Printed
MONOCULAR OF THE
in
Gr~l Britain.
EYE MOVEMENTS PIGEON1
PATRICK W. NYE Division of Applied Science, California Institute of Technology, Pasadena (Received 29 July 1968; in revised form 24 September 1968) INTRODUCTION
HEADmotion undoubtedly serves an important functional role in the visual and kinesthetic organization of the pigeon’s nervous system and it has received attention in a number of studies. DUNLAP and MOWRER (1930) showed that nictitation occurred during practically all the thrusting movements which are characteristically made during walking. Later BUYS and RIJLANT (1932) and MOWRER (1935) examined the vestibular head nystagmus in response to angular acceleration and VISSERand RADEMAKER (1934) described both the vestibular and the optokinetic head nystagmus and showed that the phenomenon remained essentially unaffected after decerebration. However, head motion is probably not the only aspect of the visual-kinesthetic response. Nevertheless, throughout all these studies, the question whether eye movements within the head make any significant contribution to the overall function of the oculomotor system was apparently overlooked. This may have been due to the fact, which is easily demonstrated by a pigeon held in the hand, that the head is sufficiently mobile to provide 360 deg visibility of its surroundings without recourse to eye movement. Thus it was possibly assumed that eye movement was unnecessary and therefore absent or unimportant. Before going on to examine the nature and role of pigeon eye movement it will be worthwhile at this point to give some detailed consideration to the structure of the pigeon eye and orbit. Of the three main types of avian eye, the globose, the tubular and the flat, the last named is found to be common to the largest proportion of birds. The pigeon possesses the flat type of eye which is encased in a tightly fitting socket and is controlled by a system of thin ribbon-like muscles. CHARD and GUNDLACH (1938) have estimated in the horizontal plane that the total field of vision of the pigeon eye is in the region of 172 deg and that the bird has a binocular visual field of about 24 deg. Thus using both eyes, visibility can be achieved over an angle of almost 300 deg. Moreover, studies of the receptor distribution in the retina have shown that the pigeon possesses a uniform densely populated mascula-like area capable of providing good acuity over a visual angle considerably in excess of the l-5-2.0 deg characteristic of the human fovea. Taking all these facts into account, the authors have concluded that eye movements must be of little importance in extending the visual field. It therefore appears that both the mobility of the head and the geometry of the eyes obviate the necessity for large eye movement; nevertheless, it is probable that some eye 1This research was supported by the National Institutes of Health USPHS Grant NE 03627. 133
131
PATRICK w.
NYE
movement is required for the important function of maint~n~g acuity. Numerous studies of human observers by D~TCH~URNand CISSBORG (19.52), Rr~cs et al. (1953), D~~CHBURNet al. (1959), BARLOW(1963) and many others have demonstrated that small involuntary eye movements serve to sustain good acuity by ensuring that the retinal receptors receive a constantly fluctuating stimulus along contours and boundaries in a pattern and are not permitted to suffer the adaptation effects which occur with stationary or near stationary retinal images. The involuntary eye movements of a normal fixating human subject are bounded within an area of diameter 30 min arc and are not usually visible to the naked eye of an observer. However, despite the fact that the pigeon would ostensibIy appear to have Iittle use for large eye rotation, it can usually be seen by relatively casual observation to make very active eye movements. This fact has been noted by a number of authors, among them WALLS(1942) and POLYAK(1957). In addition, MATURAXA(1962) observed that decerebrate pigeon preparations make rapid oscillatory bursts of eye movement at periodic intervals, but, in view of the acute condition of the animal, it was not certain whether these oscillations had any relationship to the eye movements of a normal bird. It is possible to hypothesize that, to a first approximation, head motion in the pigeon serves the same purpose as does the large voluntary eye movement of the human observer whilst small oscillations of the eyeball in its socket may be present which correspond to the involuntary physiological nystagmus of the human eye. FoIlowing a recent study of the binocular visual acuity of the pigeon (NYE, 1968) some observations on eye movement were made to examine this hypothesis and to indicate the degree to which the possible presence of a physioIo~ca~ nystagmus could infiuence the contrast threshold for a repetitive pattern. The present paper reports some measurements which have been made upon the monocular eye movements of intact partially anaesthetized pigeons and of normal pigeons. METHOD The movements of the eye were recorded by means of a beam of light reflected from a mirror attached directly to the eye. Mirror attachments were made to the left eye at the posterior rim of the cornea with the mirror center located on the horizontal meridian. Each mirror was a 4-5 mm2 aluminized chip cut from a No. 1 microscopeslide and WeiotKd about 4 mg. A powder type of denture adhesive (Corega Chemical Co.) was used to secure the mirror firmly. Figure 1 shows the design of the optical system. Light from a point source S & transmitted by the Iens Lt to form a collimated beam which iUuminates the horizontal and vertical sIIt aper&ues of the target at T. In its turn T is situated at the focus of a lens La which forms an image of S on the mirror Mt attached to the eye. Upon refiection from Mt the beam is directed by the beam splitter B through the iens L3 which formf an image of T in the pIane of a pair of triangtdar apertures placed at A. The light passing through the two sections of the mask is routed to two sqmte phot~rn~tip~ tubes (PMH and PMv) which am positioned with their cathodes in conjugate image planes, formed by the lens I.+ with respect to the mirror Ml. Crosschannel rejection (between the horizontal and vertical channels) to better than 40 db was achieved by the introduction of polarizers at T with their axes of polarization aligned with the individual slits: analysers PH and Pv were orientated perpendicularly in such a way as to block the unwanted signals. The total available field of the optical -tern was about 7.5 deg. Signals from the photo-multiplier tubes were amplified, sampled, converted into digital form and recorded on magnetic tape together with the calibration curves required to convert to angular measure. The intrinsic noise Ievel of the overail system was 12 YX arc (RMS) for the horizontal channel and 8 see arc (RMS) for the vertical channel. The tracings of eye position were obtained by means of a simple computer algorithm. The pigeons were securely held by the head with a beak clamp and ear bars, foilowing the usuat stereotaxic procedure, and orientated with respect to the horizontal and vertical axes of the optica system as shown in Figs. 1 and 2. In ail but a few experiments the p&eons were initially anaesthetized with HaIothane and, for convenience; stied in that condition untif the head had been secured, the mirror Mi attached to the eye and the bird positioned correctIy in the apparatus. Apptiitioo of the anaesthetic was then discontinued and the bird aifowed to recover whilst eye movement recordings were
The Monocular Eye Movements of the Pigeon
135
A ?MV h TO COMP!J TE?
FIG. 1. Above: Schematic diagram showing the position of the bird in relation to the principal axes of the optical system. Below: Rectangles T and A illustrate the target apertures at T with Polaroid filters attached and the triangular apertures at A on which the image of T is formed (see text). being made. In all cases a local anaesthetic was applied to the ears and a 10 per cent cocaine solution applied to the left eye. Also, to prevent blinking movements from dislodging the mirror, the nictitating membrane was removed several weeks prior to the experiments and the upper and lower lids were held apart by retractors. Approximately half of the pigeon’s left, horizontal visual field was obscured by the apparatus whilst the binocular and a portion of the lateral visual field remained unhindered. A total of six birds were examined in the eye movement apparatus. VERTICAL AXIS
i
HORIZONTAL \
AXIS
F
SUPPORT
FIG. 2. The position
of the head relative to the horizontal
and vertical axes of measurement.
136
PATRICK
W. Nn
RESULTS
A representative example of eye movement sampled at a rate of 250 per set and recorded whilst under partial anaesthesia is shown in the upper half of Fig. 3. Short
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Fro. 3. Above: Horizontal (Ii) and vertical (V) components of the eye movement of a partMy amuathetkgi &eon. +&w: Eye moveymnt fron? the same bird following recovery anac&wa. Note unpuhe in lower r&t-hand comer.
bursts of oscillation at a frequency of 27 Hz and peak to peak amplitude of l-5 deg occur at intervals of about l-3 set with the addition of some occasional impulsive movements. One of these impulses is shown following the second oscillatory burst in Fig. 3. The lower half of Fig. 3 shows a record taken from the same bird about 15 min later when it had fully recovered. The osciliatory bursts have substantially increased in amplitude reaching a peak to peak level of 5 deg when resolved in the vertical direction. A vertical impulse whose amplitude exceeds 1.6 deg is shown in the lower right-hand corner of Fig. 3 and is of interest for the fact that, although it indicates a movement whose velocity is comparable with that found during oscillatory motion, there is nevertheless no subsequent oscihation. The nature of this movement is therefore different and it is seemingly made under the restraint of an overdamped control system. Apparent tracking eye movements were also observed but only during the uide awake phases of experimental sessions. These were slow drift movements of eye position from one fixation point to the next at a rate of approximately l-5 deg/sec with total excursions in the region of 3-5 deg but sometimes exceeding the maximum range of the recording system (7.5 deg). Figure 4 shows the response to a small light source moving in the horizontal plane. Whilst it cannot be said that the precision is high there is more than a suggestion that the eye is following the target. Active eye movement of this type would occur reliably only if the target motion was irregular. Periodic motion to and fro would commonly lead to a rapid loss of interest which could be rearoused by a sudden change or cessation of the target motion. Bearing in mind the fact that the head was immobile, the data indicated that there are some ocuiomotor functions which can be
The Monocular
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137
Eye Movements of the Pigeon
k
;
;
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5
6
TIME (SECONDS)
FIG.4. Eye movements
made by a pigeon in response to a self luminous target 8 mm in diameter moving in the anterior visual field at a distance of 30 cm from the eye. Target motion is indicated by the lowermost trace and a downward deflection represents movement
in the posterior direction. expressed by eye movement although they may not operate in quite this way in the normal bird. It is, however, certain that the eye can respond more rapidly than the head and it was in response to a rapid change in the target that a pattern of movement closely resembling the flick, observed frequently in human eye movement, wouId occasionally occur. A flick, which is a rapid change of fixation taking place in less than 20 msec, can be seen in the upper left-hand corner of Fig. 4. However, the frequency of occurrence of these movements was very low, an observation which contrasts sharply with what is known of human eye movement under similar conditions (DITCHBURN and FOLEY-FISHER, 1967). Moreover, unlike that of the human observer, the pigeon eye appears to have very little physiologica tremor for it was not possible to detect it above the intrinsic noise level of the measuring system. The recording of an oscillatory movement shown in Fig. 5 was sampled at a rate 5HORIZONTAL
Y
g3 E a’
VERTICAL
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(SECONDS)
FIG.5. An oscillatory burst of eye movement shown against an expanded time scale.
of 2500 per set and shows the structure of the oscillatory wave form in more detail. The burst of oscillation itself was used to trigger the sampling process, and the section of the record preceding the crossing of the trigger threshold has inevitably been omitted. In Fig. 6 the horizontal and vertical waveforms of Fig. 5 have been plotted
138
w. NYE
P.MRICK
ANTERIZR
POSTERIOR !
0
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FIG. 6. A plot, in angular space, of the motion shown in Fig. 5. Approximate of the principal eye muscles are also indicated.
positions
against each other to give a trace of eye position in angular space. Surrounding this plot is a plan of the approximate directions of action of the principal eye muscles. The motion of the eye is seen in this case to be an elliptical spiral. In each of five pigeons examined, the trajectories have all been roughly elliptical (although not always describing as well defined a spiral as chat shown) and with their major axes rotated from 20430 deg anti-clockwise from the horizontal meridian. The frequency of the oscillation was found to range from 28-35 Hz and to be sustained for periods of up to O-8 sec. Starting points and terminal fixation points for an oscillation were seldom the same except when under partial anaesthesia. Usually the visual axis would either drift back, over a period of l-2 set, to the position originally occupied or remain at the new fixation point. The form of the decaying oscillation initially suggests the idea that it is the impulse response of an inertial load suspended from a system of passive underdamped elastic muscles. However, this appears to be an over simplification. In fact there is some evidence which indicates that much of the response is under voluntary control. Firstly, as shown in Fig. 7, occasional pulses are observed in which the oscillation is interrupted
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FIG. 7. A typical interrupted oscillatory movement which illustrates that the eye motion is not a ringing response to a single impulse but apparently under continuous control.
The Monocular Eye Movements of the Pigeon
139
for a period of about O-1 set and then continues. Secondly. it is found that the rate of decay can fluctuate from pulse to pulse and also within a single pulse. Finally, some pulses begin with relatively small excursions, climb rapidly in amplitude within two or three cycles and decay slowly over the course of a further ten cycIes. This is not the type of behavior to be expected from a passive mechanical system which has fixed parameters. To achieve such a response, either the damping applied must be controlled and vary widely from large values in the case of an impulse movement or flick to a range of underdamped values during the oscillatory pulses or, the eye muscles must be capable of exerting a flexible variety of force patterns upon a permanently overdamped system. It is convenient for the purpose of discussion to summarize these observations under a list of categories some of which were originally adopted to describe human eye movements (DITCH~URNand GINSBORG, 1953) but the use of these categories should not be taken to imply that the eye movements are identical in the two cases. Flicks are observed in fully conscious alert pigeons particularly when responding to target motion. However, the frequency of flicks relative to similar events in human eye movements is extremely low and it is possible that in an unrestrained bird this visual function is served to some extent by head motion. Impulse movements occur more frequently than flicks. Their amplitudes range up to 2 deg. Nevertheless they do not stimulate oscillatory activity and are therefore under a different mode of control. Drifts occur when there are objects moving in the visual field. They commonly take the form of movements between fixation points with velocities of about l-5 deg per sec. Tremor is not visible above the intrinsic noise level of the recording system and must lie below 12 set arc (RIMS). Oscifluhzs of the pigeon eye occur in short bursts at rates of about 30 Hz and with amplitudes of severat degrees. There is evidence that indicates that this motion is under active control and the rate of the oscillation is all the more remarkabIe when it is recalled that the maximum frequency at which human eye movements of comparable amplitude can be made is no more than 2 Hz (FENDERand NYE, 1961). DISCIJSSION
A considerable body of data on the involuntary eye movements of human subjects and their role in maintaining long term acuity has been gathered in recent years. It has been shown by DITCHBURNet al. (1959) that the eye movements which provide the most effective stimuli to the human visual system are rapid saccadic deflections of the visual axis called flicks. Studies of the fine tremor motion, which is also present, suggest that this component, summed over all frequencies, couId contribute to the m~ntenan~e of acuity although the evidence is not strong and the effect likely to be small. Setting aside the gross rotational movements, one could have reasonably expected that some saccadic eye movement would be found in the pigeon because it may be assumed that the mechanisms in the human eye which adapt to stationary retinal images also exist in the eyes of other vertebrates. However, the variety and scale of the pigeon eye movement is so different from that found in the human that it is difficult to interpret the function of its various components in quite the same terms. Much of the eye motion which can be said to resemble human involuntary eye movement is carried out voluntarily by the pigeon when stimulated by some moving object. Thus the fact that flicks have been found to occur relatively rarely, probably reflects the limited interest which the experiment holds for most pigeons rather than the degree of activity to be expected from an unrestricted bird.
140
PATRICKw. NYFi
Impulsive movements are much more common. They range up to 2 deg in amplitude and also appear more numerous under conditions of visual stimulation. In partially anaesthetized birds impulse movements were observed at intervals of about 30 set and increased in frequency, with progress toward recovery, to rates of approximately one in 5 sec. Comment on the origin of this component will be postpdned to later in the discussion. Efforts to identify significant tremor motion have not been successful and this component, which must exist at some level, lies below the intrinsic noise of the recording system. ‘IX implies that the amplitude is less than the intercone spacing for fovea1 vision (about 30 set arc). Moreover, on the basis of the data reported by DWHBURN et al. (1959), such small movements would be totally ineffmtive in stimulating the visual system of a human observer and p~sumab~y this is also true for the pigeon. An explanation of the origin and purpose of the oscillatory movements is required at this point and several questions come naturally in the following order. The first questions are concerned with artifacts. Is the motion a peculiar consequence of unusual stimulus conditions or of physiological stress generated by the experimental procedure? Two of the most important questions in this vein have been examined. The first concerns the possibility that the motion is brought about by scattered light, casting onto the retina a shadow of the edge of the mirror attachment, in such a way that the loop gain of the visual feedback obtained when tracking this stimulus is increased. This could cause the ocuiomotor system to enter a region of instability (FENDERand NE, 1961) giving rise to the oscillation. However, observations made with infra-red light have shown the response to be unchanged. Another possible source of artifact is that the pressure exerted by the stereo&& ear bars might create a disturbance of the v~tibu~ar system and thus generate a form of nystagmus. Nevertheless, it has also been possibte to dispose of this speculation by reference to the results of experiments performed upon two cooperative unanaesthetized pigeons restrained only at the wings and legs and allowing free movement of the head. Several oscillatory bursts were recorded together with most of the salient features previously described, hence, vestibular interference is not involved and the conclusion must be drawn that the oscillations are a part of a normal behavioral pattern. The next questions revolve around whether the motion is directly related to an act of visual discrimination or merely serves some peripheral function. Attending to the first point, it is clearly difIicult to reconcile such farge and rapid movements with purposeful visual scanning although there is evidence which suggests that they are under some degree of control. On refiection, therefore, it appears more likely that the osciitation has an indirect function related to the act of blinking and this conclusion is supported by the following additional data. The use of a topical anaesthetic and eye lid retractors during the recording of eye movements destroys the opportunity to observe the timing of blinks directly and the restraint placed upon head movement makes it impossible to determine precisely where the oscillatory eye movements fit into an overall activity pattern. In an effort to overcome some of these difficulties and obtain observations in conditions more closely resembling the normal state, bipolar electrodes made from 0*076 mm dia. teflon-coated platinum iridium wire were inserted into the orbits of the Ieft eyes of two pigeons in the region of the superior oblique and rectus muscles. Electrode leads were then attached to a strip connector (Microdot) fixed onto the skuf! with size O-80 x 0.125 in. stainless
141
The Monocuiar Eye Movements of the Pigeon
steel bolts and Caulk grip cement. Simultaneous recordings of eye movements and muscle potential signals were then made. A short segment of a recording is shown in Fig. 8(a). Oscillatory bursts were always accompanied by sustained muscle activity
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FIG. 8(a).
The upper three traces were recorded simultaneously and show the horizontal and vertical components of eye movement (scale shown at left) together with the corresponding muscle potentials (Mf obtained from electrodes inserted into the orbit. (b). The lower pair of traces have been selected from simultaneous recordings of the eye muscle potentials and a time of event switch (B) attached to the upper eye lid.
whilst impulsive movements were associated with substantially shorter periods of muscle action. In a supplementary group of experiments a switch was constructed from O-1 mm dia. tinned copper wire and attached to the left eye lid of an unresir~ned bird in such a way that a blink closed the contact and provided a time of event signal with very little hinderance to eye lid performance. From further recordings of eye muscle potentials made whilst walking and feeding it was an easy matter to identify the sustained muscle activity which indicated oscillatory eye movements. Figure 8(b) shows a pattern which was repeatedly demonstrated, namely that each sustained burst of muscle activity was precisely correlated with a blink. Shorter bursts of muscle activity presumably associated with impulse movements were also often accompanied by blinks but the correlation was not high, possibly because the switch failed to respond to short high speed motion. Thus the results showed that some impulse movements and a substantial proportion, if not all, of the oscillatory activity normally occurs during a blink. The most commonly accepted function of the blink reflex is that given by SLONAKER (1918), namely, that the nictitating membrane keeps the cornea free from dust and other foreign matter. It would therefore seem probable that the purpose of the eye motion is to provide a polishing action between the cornea and the papiliary lining of the nictitating
hITUCK W. NYFi
142
membrane. However, there is another possible functiou of nictitation which has been suggested by DUNLAP and MOWRER (1930). They observed a close correlation between nictitation and head movement and concluded that the membrane may blank out or suppress vision during the motion and hence sustain the percept of world stability. In view of this proposal it is interesting to note that in Fig. 8(b) and elsewhere, the period of a blink is almost always shorter than the period of the corresponding muscle action and it is apparent that the eye is still in rapid motion when the blink has been completed and the eye fully opened. Whether this is a normal behavioral response, or represents a lack of coor~nation which disappears when the animal is in more congenial surroundings, is difficult to determine; but if the data do indicate the true sequence of events the oscillating visual image could be highly confusing unless centrally compensated by precise proprioceptive or motor outflow information. Either one or both sources of information could be available but in their absence it is conceivable, as suggested by RICHARDS(1968), that a degree of suppression couid result from a depoiarisation of the retina caused by the action of shearing forces between the retina and the vitreous generated during the oscillation. It is apparent from this discussion that the evidence as a whole points to the conclusion that the oscillatory component has no direct role in visual discrimination and indicates that although the rotational range of the pigeon eye is smaller than our own, it possesses, in contrast to what is often assumed, a well developed oculomotor system capable of generating a repertoir of eye motion which in some respects exceeds our own in speed and agility. Moreover, one final remark should be added, namely, that from the practical viewpoint of the electrophysiologist working on the visual system of an acute pigeon preparation it is clear that the risk of artifact arising from such large eye movements as those reported here is very high and the mobility of the eye can no longer be ignored or its immobility tacitly assumed. REFERENCES
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DITCHBU~N,R. W., FENDER,D. I-i. and MAYNE, S. (1959). Vision with controlled movements of the retinal image. J. Physiot. 14!5,9&107. DXTCHBURN,R. W. and FOLEY-FISHER, J. A. (1967). Assembled data in eye movements. Uptica Acta 14, 113-l IS. DUNLAP, K.
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MA-A, H. R (1962). Functional organization of the pigeon retina. In: Information Processing in the Nervous System. (Proc. XXII International Congress, Leiden, 1960) pp. 170-178. Movvaazt, 0. H. (1935). The nystagmic response of the pigeon to constant angular acceleration at Iiminal and supmliminal intensities. J. camp. Psychol. 19, 177-193. NYE, P. W. (1968). The binocular acuity of the pigeon measured in terms of the modulation transfer function. vision Res. 8, 1@41-1053. PoLYAK,S. L. (1957). 27zeVertebrate Visual System. Univ. of Chicago Press, Blinois. RICHARDS, W. A. (1968). Visual suppression during passive eye movement. J. opt. Sot. Am. 58,1159-l 160.
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of the Pigeon
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RIGGS, L. A., RATLEF, F., CORNSWEET, I.D. and CORNSWEET, T. N. (1953). The disappearance of steadily fixated visual test objects. 3. opt. Sot. Am. 43, 495-501. SLONAKER, J. R. (1918). A physiological study of the anatomy of the eye and its accessory parts of the English sparrow. J. Morphol. 31, 351450. VISSER,J. and WEMAKER, G. G. J. (1934). Die optischen reaktionen grosshimloser tauben. Mitteilung I. Archs N
Abstract-The monocular eye movements of both restrained and partially restrained pigeons have been measured by means of a mirror attached to the edge of the cornea. The principal observations may be summarized under the following categories. Flicks, or eye movements which bring about a rapid change of fixation, are found to occur only in response to sudden and unexpected motion of a visual stimulus and are rarely observed under the quiescent conditions of a darkened room. Drips, which are slower movements of the eye between fixation points, occur at velocities of about l-5 deg per set and are stimulated by object motion. Tremor motion is of extremely low amplitude and is unlikely to serve any visual function. Oscillarions occur in short bursts at frequencies of about 30 Hz and amplitudes of several degrees. The evidence indicates that this eye movement is normally executed during a blink and it is probable that it performs a polishing action on the cornea in conjunction with the nictitating membrane. The observations lead to the conclusion that although the range of rotational motion available to the pigeon is less than in man, it nevertheless possesses a well developed and precisely controlled oculomotor system which appears in some respects to out-perform our own. Resume-On mesure les mouvements monoculaires des yeux du pigeon par un miroir fise au bord de la comee. On peut resumer les principales observations sous les categories suivantes. Mouvements rapides de changement du point de fixation, ne se produisant qu’en reponse a un mouvement soudain et inattendu du stimulus visuel, et rarement observes dans le calme dune chambre sombre. DPrives, mouvements plus lents de l’oeil entre des points de fixation, avec des vitesses de 1 A 5’ par set et stimults par le mouvement de l’objet. Tremblement de t&s faible amplitude, probablement sans fonction visuelle. Oscillations, par bouffees courtes ;i des frequences voisines de 30 Hz et des amplitudes de quelques degrts. 11 semble que ce mouvement de l’oeil se produise normalement pendant un clignement et serve probablement a polir la comee, en conjonction avec la membrane nictitante. De ces observations on conclut que, quoique le domaine de rotations possibles soit moindre pour le pigeon que pour I’hornme, il posstde cependant un systtme oculomoteur bien developpe et control6 avec precision, systtme qui g certains points de vue semble surclasser le notre. Zusammenfassung-Die monokularen Augenbewegungen sowohl von hxierten als such von teilweise ftxierten Tauben wurden mit Hilfe eines Spiegels gemessen, der am Rande der Hornhaut befestigt war. Die hauptsichlichen Beobachhmgen konnen in folgenden Kategorien zusarnrnengefal3t werden. Flicks oder Augenbewegungen, die eine schnelle Verlnderung der Fixation bewirken, wurden nur als Reaktion auf eine schnelle, unerwartete Bewegung eines visuellen Reizes gefunden und werden selten unter den ruhigen Bedingungen eines verdunkelten Raumes beobachtet. Drifbewegungen, das sind langsamere Augenbewegungen zwischen den Fixationspunkten, die mit einer Geschwindigkeit von ungefahr l-5 Grad pro Sekunde auftreten, werden von der Objektbewegung hervorgerufen. Zitter-Bewegungen weisen eine garu besonders niedrige Amplitude auf, und es ist unwahrscheinlich, daB sie irgend einer visuellen Fur&ion dienen. Schwingungen treten in kurzen Ausbriichen mit Frequenzen von ungeflhr 30 Hz und Amplituden von mehreren Grad auf. Der Augenschein zeigt, da0 diese Bewegung norrnalerweise w&rend eines Lids&lags ausgefiihrt wird, und es ist wahrscheinlich, daB sie, zusammen mit der Nickhaut, eine polierende Wirkung auf der Homhaut bewirkt.
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