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Exp Brain Res (2001) 139:173–179 DOI 10.1007/s002210100774 R E S E A R C H A RT I C L E Matthias Ott Chameleons have independent eye movements but synchronise both eyes during saccadic prey tracking Received: 31 January 2001 / Accepted: 9 April 2001 / Published online: 16 May 2001 © Springer-Verlag 2001 Abstract The movements of both eyes and the head were recorded with search coils in unrestrained, freely moving chameleons. As a main result I found that the generation of saccades in the left and the right eye was either independent from each other or was highly correlated according to the behavioural situation. When no prey item was fixated, disconjugate saccades were observed which was in accordance with earlier observations in chameleons. During prey tracking the chameleons switched to a different oculomotor behaviour and pursued the moving prey with synchronous saccades. At higher target velocities, the tracking movement of the head was also saccadic and was synchronised with the two eyes. Binocular coupling affected only the timing of the saccades but not the metrics: the amplitudes of the synchronous saccades were usually different in the two eyes. These observations suggest the existence of two independent premotor neuronal circuits for left and right eye saccadic motor control in the chameleon. Binocular coupling in prey-tracking chameleons is probably achieved by neuronal coupling of these premotor circuits during eye–head coordination. The ability to switch between synchronous and uncoupled saccadic eye movements has not been described for any other vertebrate. This unique ability of the chameleon may help to understand the organisation of the oculomotor system of other vertebrates since evidence for separate left eye and right eye saccade generation and position control has recently also been reported in primates. Keywords Chameleon · Independent eye movements · Binocular coupling · Saccade generation · Eye–head coordination M. Ott (✉) Institute for Anatomy, University of Tübingen, Österbergstrasse 3, 72074 Tübingen, Germany e-mail: [email protected] Tel.: +49-7071-2973026, Fax: +49-7071-2974014 Introduction In human vision, the perception of depth (stereopsis) requires synchronous initiation of left and right eye movement in order to maintain binocular fuse of the two retinal images. Early investigators believed that synchronous binocular coordination in humans was the effect of motor commands that induce movements of the two eyes simultaneously (Hering's law of equal innervation; Hering 1868). von Helmholtz (1896) was the first who recognised that movements of the two eyes could be different from each other and also be influenced by learning. He concluded that separate motor commands must be sent to the left and the right eye. Recent findings support the theory of Helmholtz. Dell'Osso (1994) described a genetic defect in dogs, where the affected individuals moved their eyes independently, while unaffected siblings showed conjugate eye movements. Zhou and King (1998) reported that premotor neurons in the paramedian pontine reticular formation of macaques which were thought to encode conjugate velocity commands for saccades actually encoded monocular commands for either right or left eye saccades. The study of non-mammalian vertebrates also suggests that the basic organisation of the oculomotor system is monocular with separate motor commands for the two eyes. Independent eye movements are common in fish and lizards (Walls 1961; Kirmse 1988), while many birds show unequal amplitudes when moving both eyes (Wallman and Pettigrew 1985). Comparative studies revealed no obvious anatomical differences in the relevant brainstem structures of vertebrates that could explain the differences in ocular movement control (Evinger 1988). If the basic organisation of the oculomotor system is monocular, synchronous eye movements, like those in primates, may have developed by neuronal coupling of the symmetrical oculomotor structures. A first step would be to synchronise the timing of eye movements so that saccades start simultaneously. Interestingly, such a stage of binocular coordination seems to be represented in the oculomotor system of the chameleon. These lizards move their eyes over a range of more than ±90°, and do so for 174 each eye independently. The results presented here show that chameleons are able to switch from independent saccadic eye movements on the one hand to strictly synchronised eye and head movements during prey tracking on the other hand. The eye of the chameleon is an interesting model for oculomotor research. Similar to primates, it has a central fovea and performs saccadic fixation movements. The high ocular mobility enables the chameleon to overlap the visual fields of both eyes completely during prey fixation. Although now both eyes look forward as they do in primates, stereopsis is not used to judge distance. Rather, the chameleon uses the cues coming from the amount of ocular accommodation for distance estimation (Harkness 1977; Ott et al. 1998). Visual resolution is high due to a dense photoreceptor package (756,000 cones/mm2) in the all cone retina (Pütter 1912, cited in Franz 1934). Unique among vertebrates, the eye lens is of negative refractive power which elongates the focal length and, as a consequence, creates a larger retinal image (Ott and Schaeffel 1995). This improves visual resolution during monocular depth perception and, hence, the precision of the tongue strike by which the chameleon catches its prey. Materials and methods Animals A total of seven captive-bred Chamaeleo calyptratus or wildcaught C. dilepis were used in this study. The animals had a snout–vent length of 10–12 cm. They were housed in well-ventilated cages equipped with heating light bulbs and fluorescent illumination. The chameleons were fed with insects, mainly flies and crickets. The main set of experiments was done with two very tame C. dilepis. The remaining animals did not adjust to handling during experiments and allowed only qualitative observations. Fig. 1 Flap-neck chameleon (Chamaeleo dilepis) wearing a search coil on its eye lid and on the head. Coils were glued on the temporal rim of the lid with water-soluble glue. A stiff piece of cardboard was used to carry the head coil and was fixed firmly onto the head with adhesive tape Methods Eye movements were measured in the horizontal plane by using a commercially available search coil system with large-diameter field inducing coils (Angle-Meter; Primelec, Zürich, Switzerland). The system was based on the phase detection principle (Collewijn 1977; Kaspar et al. 1987). A rotating magnetic field vector of constant magnitude induced an alternating voltage signal whose phase value depended linearly on the angular orientation of a small measurement coil (search coil) which was fixed to the eyes or to the head of the animal. The spatial resolution of the system was ±1° in the horizontal plane. This angular resolution could be maintained within a diameter of about 20 cm within the centre of the magnetic field and allowed the chameleons to follow moving prey with head or body movements. Search coils were either hand made or obtained from Sokymat, Granges/Veveyse, Switzerland. The coils had long (1 m) twisted leads to allow movements of the animal and had an average resistance of 38 Ω. Using water soluble glue the coils were firmly attached to the rim of the eye lids and/or directly onto the head just before the beginning of a trial and were removed at the end of each session (Fig. 1). Care was taken not to restrict the movements of the eye by the rigidity of the coil or a surplus of the glue. After the coil has been fixed, the chameleon was observed for several minutes and experiments were only proceeded if the animal showed no signs of discomfort or restriction of eye movement. Head coils were glued to a small piece of stiff cardboard which was fixed to the head with adhesive tape. The chameleons were then placed on a perch within the centre of the magnetic field (Fig. 2). Crickets were presented by forceps and held either stationary in front of the chameleon or were moved by hand sinusoidally in a plane perpendicular to the mediosagittal plane of the chameleon. The chameleons were videotaped from above to correlate the observed behaviour with the search coil data. After A/D conversion, the search coil recordings were analysed with a personal computer using a custom-made program written by Eurotronics, Leipzig, Germany. The system allowed simultaneous recording of two coils with a scanning rate of 200 Hz/channel. Velocity profiles were calculated from the slopes of the straight lines between neighboured data points and low-pass filtered. Saccade onsets were determined by velocity and acceleration criterion for both eyes and the head. For data analysis, the temporal coupling between both eyes was described by cross-saccadic intervals, defined as the time span between saccade onset in one eye (the reference eye) and the onset of the nearest saccade of the other eye. 175 Fig. 3 Horizontal components of binocular eye position during spontaneous eye movements in a chameleon. Both position traces represent gaze, i.e. minor movements of the unrestrained head are included in the eye coil signal. The movements of both eyes are independent from each other. Note that for a certain period of time large saccades are usually seen in only one of the two eyes while the other eye keeps its position relatively constant Fig. 2 Experimental set up for the search coil recordings of eye and head movements in unrestrained chameleons. Chameleons were placed on a wooden perch into a magnetic field that was produced by a cubic arrangement of the square-shaped primary coils. Two recording coils were either glued on each of the two eyes or on one eye and the head. The twisted leads of the recording coils were directed to a wheel on the top of the cubic primary coils. On the other side of the wheel the leads were supported by a small weight that was just heavy enough to keep the lids tight without restraining the movements of the animal. Crickets were offered by hand-held forceps. The movements of both the chameleon and the bait were videotaped from above Fig. 4 A sequence of eye position traces. Both position traces represent gaze, i.e. movements of the unrestrained head are included. The left eye was directed to a forward-looking position to fixate the prey. The right eye was in a lateral position and was still moving around in the lateral field with some large saccades. At the moment of binocular coupling the right eye rapidly converged with the left eye to achieve binocular prey fixation. The head (as revealed by the video tape, not shown) was moved towards the prey together with the right eye and was then kept in constant position during eye convergence. At the moment of the tongue shot (ts) both eyes quickly diverged to lateral positions and the eye lids were closed. This is a protection reflex to prevent any damage of the eyes from the struggling legs of the prey when the tongue is withdrawn Results Technical concerns The search coils were not implanted into the eye but glued onto the rim of the eyelid. This could cause slippage of the coil relative to the eye ball and, as a consequence, affect the precision of the recorded signal especially for highly accelerated movements such as saccades. Previous studies, however, showed that the eye lids are attached firmly by muscles to the eyeball in chameleons and, therefore, follow the rotations of the eyeball without angular slip (Sándor et al. 1997; Ott et al. 1998). Direct comparison of lidglued and implanted coils did not reveal any differences in the recorded signal (Sándor, personal communication). Chameleons are very shy and stop prey-catching behaviour immediately if they are restricted or manipulated during the experiment. The ability to learn is very limited and the animals can not be trained to adjust to experimental procedures, such as head fixation. Therefore, only unrestrained animals could be observed. As a consequence, the signal of the eye coils included also head movements and represent “gaze” rather than eye position. By comparing the peak velocities of head and eye coil signals it was possible to estimate that the average head component in the signal of the eye coil was about 40% (Fig. 9). Peak velocity of the eye coils, measured during prey tracking, was directly correlated with the amplitude (Fig. 8). Visuomotor response to stationary prey items In the absence of prey the chameleons looked around with independent, large-amplitude saccadic eye movements (Fig. 3). For a period of one or several seconds saccades were often seen in only one of the two eyes while the other eye kept its position relatively constant. Prey items presented to the chameleon were initially detected monocularly. When the animal decided to catch the prey, a combined movement of the head and the contralateral eye was initiated towards the target to achieve binocular prey fixation. Prior to binocular fixation, the contralateral eye often scanned the environment with several large-amplitude saccades (Fig. 4). During binocular prey fixation, the eyes converged (Fig. 5). These convergence movements were smooth but could include small synchronous saccades (Fig. 5b, c). Eye convergence was not correlated with prey distance since it could also be observed when the animal kept its distance towards the prey constant. 176 of the head saccades was also the same as in the synchronous eye saccades but with lower peak velocities. Head saccades occurred only during relatively high prey velocities. Slowly moving prey was tracked with smooth head movements with no apparent head saccades in accordance with earlier observations (Flanders 1985). Quantitative analysis of eye and head saccades Fig. 5a–c Binocular convergence shortly before the tongue shot (ts) is visible in these position traces for the two eyes in three independent trials. After both eyes have been directed forward they keep on to converge to each other (note the stippled difference curve). Internal coupling of the two eyes was probably achieved only very shortly before the tongue shot in a but can be recognised by small synchronous converging eye movements in b and c (arrowheads). Both position traces represent gaze as in Figs. 3 and 4. The head position (recorded by video, not shown) was constant except for minor turns around the mediosagittal line Visuomotor response to moving prey In these experiments, the prey was moved back and forth in a line perpendicular to the mediosagittal plane in front of the chameleon. The chameleons tracked these sinusoidal prey movements mainly by head movements, as described earlier by Flanders (1985). However, in contrast to that study I found that the eyes were not locked with respect to the head. Rather, they pursued the moving prey with sequences of small saccades (Figs. 6, 7). The generation of these saccades was strictly synchronous in the two eyes which was in contrast to spontaneous vision when both eyes move independently from each other. The synchronism of saccades is expressed by the close range of the cross-intersaccadic intervals, defined as the time span between saccade onset in the reference eye and the onset of the nearest saccade of the other eye (Fig. 6d). The majority of intersaccadic intervals were in the range of 0 or 10 ms. Sometimes, a typical saccade in the one eye was associated by a saccade-like signal (but without the typical acceleration profile) in the other eye that could not be used for calculation of the intersaccadic interval (see first pair of saccades in the enlarged graph at the bottom of Fig. 6). In these cases, the clear signal was counted as an unpaired saccade (Fig. 6d). Very few saccades were clearly monocular with no signal in the other eye. In a second set of experiments, the coordination between the movement of the head and one eye was investigated (Fig. 7). At given stimulus velocities (peak velocity about 60°/s in Fig. 7) head saccades were observed that were synchronous to those of the eye. The direction As shown in Fig. 8, the peak velocities of the saccades could be linearly correlated to the amplitude. Signals from the eye coils represented gaze, i.e. the combined movements of the eye and the head (gaze). Head-fixed recordings of eye position traces were not tolerated by the chameleons. Therefore, it was necessary to exclude that the synchronism of eye saccades, as shown in Fig. 6, was only the effect of underlying head saccades while the eyes did not make saccades at all. According to the calculations in Fig. 9 this explanation is unlikely to be true. Peak velocities recorded by the eye coils were larger than the head coil signals. A relation of the peak velocities of synchronous saccades in the two eyes showed a linear correlation with a slope equal to 1 (y=17.67+ 1.001x; r2=0.951). The relation of peak velocity of the eye coil compared to the head coil was also linear, but with a much lower slope of about 0.4 (y=3.66+0.387x; r2=0.803). Discussion Types of eye movements observed in chameleons Among the five basic types of eye movements described for vertebrates (Büttner and Büttner-Ennever 1988) saccades, vestibulo-ocular reflexes and optokinetic reflexes are well developed in the chameleon (Gioanni et al. 1993, 1997; Frens et al. 1998). From the remaining two types of eye movements, binocular convergence could be observed in the chameleons although it was not clearly related to the distance of the stimulus (Ott et al. 1998). Smooth pursuit eye movements were not observed at all. However, smooth pursuit might have been masked by catch up saccades due to the high stimulus velocities (30–50°/s). In humans, smooth pursuit eye movements are observed up to a maximum velocity of about 20°/s (Schalen 1980). It was not possible to record pursuing eye movements at lower prey velocities because in those cases the chameleons immediately caught the prey. Sensory-motor transformation in chameleons The aim was to detect internal patterns of visuomotor coordination without any experimental artefact resulting from fixing the head or body of the animal. The gain of eye or head movements with respect to the moving prey could not be calculated with the experimental set up, but 177 Fig. 6a–d In this sequence a hand-held bait was moved sinusoidally in a horizontal plane in front of the chameleon. Position curves (a) represent gaze as in Figs. 3, 4 and 5. The major sinusoidal displacement was due to the head movements. The prey was pursued with synchronous saccadic movements of the two eyes as indicated by the peaks in the velocity traces in b and the enlarged frame at the bottom (c). Crossintersaccadic intervals were calculated as the time between the onset of a saccade in one eye (reference) and the nearest onset in the other eye (d). Unpaired saccades, such as the first one shown in c, were counted separately. The remaining three pairs in c had time lags of 20, 20 and 0 ms. The majority of cross-intersaccadic intervals ranged between 0 and 20 ms with an equal distribution of associated saccades that preceded (negative time lag) or followed (positive time lag) the saccade in the reference eye (d) was analysed in a previous study by Flanders (1985). According to this author, the chameleons followed the prey with a time lag that varied between individuals (52.8–144.4 ms) but was not affected by bait frequency. The chameleons were obviously unable to predict the course of the prey movement. Despite the regular sinusoidal movements of the prey the chameleons did not anticipate the back-movement of the prey when it was at its peak displacement. The author did not observe any eye movements during head tracking and reported that the two eyes were invariably locked in a forward-looking position within the head. Based on this observation, Kirmse et al. (1994) described a simple neural mechanism for sensorimotor transformation in chameleons: the fixed eye position during prey tracking would allow a direct conversion of the two-dimensional position of the retinal image into a three-dimensional motor command for the head tracking movements without caring for eye position. In the present study, search coil records in chameleons revealed clear eye movements also during prey tracking that were overlooked in previous studies, probably due to the restricted temporal resolution of film and video recordings. Different to Flanders (1985), I moved the prey by hand instead of an electro-mechanical device. Due to this difference, the target was probably moved less smoothly with more abrupt incidents of retinal slip to serve as stimuli for saccades. However, a fixed position of the eyes could never be observed in all my recordings 178 Fig. 9 Comparison of peak velocity of synchronous saccades recorded by coils glued to both eyes (a) or to one eye and the head (b). Peak velocities were linearly correlated with a slope equal to 1 in the interocular comparison. This is expected if both eyes had similar average saccadic amplitudes. The slope was lower (0.4) when the peak velocity of the head and one of the eyes was compared. This indicates that rapid (saccadic) displacements in the eye coil signal were mainly due to eye movements. Data from two chameleons (C. dilepis) orienting movements in mammals, such as cats and primates (Guitton et al. 1990), and it is reasonable to assume that the basal neuronal mechanisms for gaze control in chameleons are not different to mammals. Fig. 7 Horizontal components of the position of one eye coil and the head during pursuit of sinusoidal prey movements. Note the presence of saccadic head movements which were synchronous to those of the eye coil Fig. 8 Peak velocity-amplitude relation of saccades observed during prey tracking. Data from two chameleons (C. dilepis) even during quick phases of prey movements that appeared absolutely smooth in a frame by frame analysis of the video tape. The presence of saccades during prey tracking contradicts the model of Kirmse et al. (1994) of direct conversion of the retinal image into a three-dimensional motor command. Rather, an eye position signal must be added to the retinal position signal to create an internal representation of the position of the target with respect to the head. This means that the positions of the eye and the head are summed together into co-ordinate frames that are not closely related to the geometry of the sensory organs. Similar conclusions have been drawn for Oculomotor control is separate for each eye The anatomy of oculomotor nuclei in chameleons has been analysed in a recent paper by El Hassni et al. (2000). This study revealed a highly differentiated oculomotor, trochlear and abducal nuclear complex in the chameleon brain which was similar to the organisation of the oculomotor nuclei in mammals. This similarity facilitates comparisons with the mammalian oculomotor system and, in particular, with the saccadic subsystem which in mammals is well understood in terms of its neuronal connectivity and discharge patterns (Moschovakis et al. 1998). The most remarkable result of the present paper is the observation of a behavioural switch between synchronous and independent saccades in the chameleon. The oculomotor system of the chameleon is probably an interesting intermediate model to investigate the transition from totally independent to permanently coupled eye movements in vertebrates. It is very likely that the chameleon synchronises its saccades due to an internal coupling in the neural substrate. If both eyes were just responding independently to the same external trigger, one would expect a broader bandwidth of the cross-intersaccadic intervals in Fig. 6d. Further, neuronal binocular coupling was also observed during ocular accommodation in chameleons. Both eyes usually focus independently from each other. During prey fixation, however, accommodation is symmetrical in the two eyes even if one eye is covered (Ott et al. 1998). Studies in mammals support the notion that the general vertebrate bauplan for oculomotor control is based on independent oculomotor control units for each eye separately. During sleep, rapid eye movements (REM) were found to be monocular or disjunctive with misaligned 179 optical axes up to 30° horizontally and/or vertically in the two eyes (Zhou and King 1997). Electrophysiological studies in primates revealed that premotor positionvestibular-pause neurons fire in relation to monocular (right or left) eye position rather than to conjugate eye movements (McConville et al. 1994; Zhou and King 1998). A monocular control of the saccadic system for each eye separately is further supported by studies of disconjugate and asymmetric saccades observed in normal and strabismic humans as well from observation of achiasmatic dogs (Dell'Osso 1994). In contrast to the separation of the two eyes within the premotor neuronal circuits the motoneurons of abducal and oculomotor cranial nuclei fired in response to movements of either eye in primates (King et al. 1994; Zhou and King 1998). A similar binocular convergence onto the motoneurons may also be present in some of the chameleon extraocular muscles because Frens et al. (1998) found that in these lizards the two eyes are not strictly separated from each other. These authors observed an increased likelihood for left and right eye saccades to start in close temporal proximity to each other even during spontaneous vision when no prey target was around. In context with the cited observations of binocular coupling at the level of premotor neurons it is interesting to note that in chameleons as well as in birds (Wallman and Pettigrew 1985) only the timing of saccades is yoked together whereas the amplitudes of the saccades can be different. For the chameleon this is indicated by the different peak velocities of synchronous saccades shown in Fig. 6. As shown in Fig. 8, the peak velocity of saccades was linearly correlated with the amplitude. The pattern of binocular coordination in chameleons supports the idea that in vertebrate phylogeny the movements of the two eyes are coupled by pathways that synchronise the timing of monocular motor commands for both eyes. This synchronisation does not affect neural commands on eye position as indicated by the different metrics of saccades in chameleons and birds, the different eye positions during REM sleep in mammals and, finally, the encoding of monocular eye position signals in premotor units of primates as cited above. Acknowledgements The author thanks W. Kirmse for the possibility to work in his laboratory and for helpful discussions. I further thank P. Sándor, M. Frens and two anonymous referees for valuable comments on the manuscript and to H.-J. Wagner for critical reading of the text. M. Nicolescu has illustrated the experimental set up. All experiments comply with the “Principles of animal care”, publication number 86–23, revised 1985, of the National Institutes of Health and with the German “Tierschutzgesetz”. This study has been supported by a grant of the Deutsche Forschungsgemeinschaft to M.O. (Ot 183). 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