Download Chameleons have independent eye movements but synchronise

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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