J. exp. Biol. 188, 89–101 (1994)
Printed in Great Britain © The Company of Biologists Limited 1994
89
BLIND MEXICAN CAVE FISH (ASTYANAX HUBBSI) RESPOND
TO MOVING VISUAL STIMULI
THOMAS TEYKE AND STEPHANIE SCHAERER
Institut für Zoologie (III) Biophysik, Johannes Gutenberg-Universität, 55099 Mainz,
Germany
Accepted 22 November 1993
Summary
In apparatus for measuring optomotor behaviour, blind Mexican cave fish, Astyanax
hubbsi, increase their swimming velocity upon rotation of a striped cylinder, i.e. in
response to a solely visual stimulus. The fish follow the movements of the stripes at
(i) rotation velocities between 60 degrees s21 and 80 degrees s21, (ii) light intensities of
less than 20 lx and, (iii) stimulus widths subtending an angle of less than 1 ˚.
Extirpation of the vestigial eye structures does not affect the response to the moving
visual stimulus, which indicates that the response is mediated by extra-ocular
photoreceptors.
An optomotor response can be reliably evoked in a round test aquarium. Fish do not
respond when the test aquarium contains environmental cues, such as bars on the wall or
when a section of the round aquarium is divided off. This indicates that the fish obtain
information about their environment from different sensory sources and that the visual
stimulus is effective only when no other means of orientation are available. We suggest a
modified theory of the optomotor response, which emphasizes the crucial role of the
environment in eliciting the response and which permits behaviours more complex than
just following the stimulus.
Introduction
There is mounting evidence that in various animals extra-ocular photoreceptors (EOPs)
play an important role in eliciting different behaviours (for reviews, see Underwood and
Groos, 1982; Oliver and Bayle, 1982). It was shown that experimentally blinded (and
pinealectomized) fishes respond to light (Scharrer, 1928; de la Motte, 1964) and utilize
this capacity in a behaviourally relevant manner, such as changing their skin colour
(Frisch, 1911) or controlling motor activity (van Veen et al. 1976). A few studies have
employed blind Mexican cave fish (Astyanax hubbsi), which have no superficially
discernible eye structures and thus seem to be an advantageous model for comparing the
functional role of EOPs with that of lateral eyes in fish. The remnants of the eyes, called
optic cysts, are highly atrophic and are buried deep within the tissue in the orbital region
(Gresser and Breder, 1940; Kähling, 1961; Wilkens, 1988). Blind cave fish were found to
be unresponsive to direct stimulation with points of light (Voneida and Fish, 1984), but
Key words: optomotor response, extra-ocular photoreceptors, environmental constraints, cave fish,
Astyanax hubbsi.
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T. TEYKE AND S. SCHAERER
could distinguish minute differences in ambient lightness (Breder and Gresser, 1941a;
Kuhn and Kähling, 1954; Lüling, 1954; Kähling, 1961). It was suggested that this sensory
capability is dependent upon the remnants of the eyes (Breder and Gresser, 1941b).
However, evidence that extra-ocular photoreceptors, not the eyes, are responsible for the
perception of light appears to be equally convincing (Kuhn and Kähling, 1954; Kähling,
1961). In blind cave fish, as in other fish, extra-ocular photoreceptors have been located in
the pineal organ (Herwig, 1976). Extra-pineal photoreceptors have not been identified in
blind cave fish yet, but their presence and location can be inferred from studies in other
fish (see, for example, Hartwig and Oksche, 1982; Dodt and Meissl, 1982).
It is important to keep in mind that the results of different studies on the visual
capabilities of the blind cave fish Astyanax are not immediately comparable since different
populations of cave fish, found in different pools within the cave, differ considerably in the
degree of reduction of their eyes and disorganization of the retinal structures and,
correlated to that, in their visual potential (Breder and Gresser, 1941a). Therefore, it is
imperative to determine the visual abilities of our experimental fish by comparing their
behaviour with that reported for the different populations of blind cave fish.
Blind cave fish are blind fish
Our observations indicated that our experimental fish behave in a manner typical of
fully blind fish believed to be incapable of forming a retinal image and thus having no
visual capacity (see Breder and Gresser, 1941a). (1) They swim continuously through the
aquarium; (2) they do not respond to visual stimuli, such as points of light directed at
them or shadows from above; (3) they do not school; (4) they perform a typical searching
behaviour on the bottom of the tank when food is tossed into the aquarium and (5) they
occasionally collide with objects in unfamiliar environments.
Preliminary morphological studies have revealed that the eyes of our experimental fish
are reduced to a considerable extent. A residual ‘optical cyst’ is located under layers of
fatty tissue deep within the orbital region. The eye is small (about 1 mm in diameter) and
highly atrophic: (1) the front is coated with a dark, reflective pigment; (2) there is no lens
and (3) the retina shows hardly any stratification. Serial sections indicated that several
retinal cell types are present, but photoreceptors could not be identified.
These findings indicate that our breeding stock of blind Mexican cave fish, Astyanax, is
characterized by the highest degree of optical reduction observed in blind cave fish (see
also Wilkens, 1988) and suggest that they are not able to obtain visual information by
means of their eyes.
We now report that fully ‘blind’ cave fish show a reliable behavioural response to white
vertical stripes that are rotating around an aquarium in apparatus used for testing
optokinetic behaviour. Our observations indicate that this behaviour is independent of the
eyes, suggesting that extra-retinal photoreceptors are responsible for detecting the visual
stimulus provided by the rotating bars.
Materials and methods
Behavioural testing
Adult blind cave fish of body lengths between 4 and 6 cm were kept in separate holding
Visual behaviour of blind cave fish
91
tanks. Individual fish were placed in a circular test aquarium (12 cm diameter) suspended
in the centre of a vertically striped cylinder (20 cm in diameter). The cylinder consisted of
white stripes (2 cm wide, unless otherwise noted) arranged in a regularly alternating
pattern and driven by an electric motor. A black velvet curtain provided a uniform
background and shielded the apparatus from outside light. Illumination was provided
from above, and the fish were monitored with a video camera from below.
After placing a fish in the test aquarium, it was permitted to explore and become
accustomed to the environment for 2 h. Control experiments indicated that an exploration
period of 2 h was sufficient for blind cave fish to become familiarized with their
environment, as indicated, for example, by the reduction of their swimming velocities to
low-level cruising speeds (see Teyke, 1989). After the exploration period, the
spontaneous swimming behaviour of the fish was video taped for 2 min, followed by a
recording of the same duration during rotation of the striped cylinder. Frame-by-frame
analyses of the video recordings were carried out to determine the angular position of the
fish in circular coordinates. The projection of the tip of the head (perpendicular to the
body axis of the fish) to the perimeter of the aquarium was utilized to determine the
angular position of the fish. By doing this, straight swimming and translational turning
movements of the fish were converted into a circular movement which could be measured
in degrees. These data were then used to calculate the velocity of the fish (given in
degrees s21). Based on this we computed (1) the average velocity of the fish (irrespective
of the swimming direction – with or against the turning direction of the cylinder); (2) the
average absolute velocity (which took the turning direction into account); and (3) the
error (the angle between the position of the fish and the stripe closest to it). As shown
below, the average velocity of the fish (regardless of the direction of swimming) was
found to be an appropriate measure of the fish’s behaviour. For each experiment, the
fish’s spontaneous velocity before testing was compared with that during rotation of the
cylinder. For statistical analysis of the data of individual experiments, t-tests were
employed. ANOVA was utilized for assessment of overall effects.
Animal preparation
For surgical extirpation of the eyes, the fish were anaesthetised with MS 222 (Sandoz).
A small incision was made in the skin overlying the orbital region and the optic cyst was
removed after transection of the optic nerve and connecting tissue. The fish recovered
quickly and without discernible complications from this procedure and were tested 14
days and again 8 weeks after surgery.
Results
Blind cave fish increase their velocity upon rotation of white stripes
In the experiments described below the fish were selected randomly and different
experiments were performed in a random sequence to avoid conditioning, habituation and
other unrelated effects. Experiments in which a fish swam spontaneously at velocities at,
or above, 60 degrees s21 were discontinued. Of the six experimental fish tested, one fish
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T. TEYKE AND S. SCHAERER
360
A
270
180
Position (degrees)
90
0
360
B
270
180
90
0
0
10
20
30
40
50
60
Time (s)
Fig. 1. Behaviour of a blind Mexican cave fish in response to a moving visual stimulus.
(A) Position of a fish (in degrees) in a round aquarium during spontaneous swimming. (B)
Position of the fish during rotation of the striped cylinder at 80 degrees s21. Note that the fish
attempted to keep its position close to that of a white stripe (the angular position of the white
stripe is indicated by the thin line). Arrowheads indicate where the fish fell behind one bar and
followed the next one.
was dismissed from the group after the experiments had been completed, because it
increased its velocity during two control recordings.
A good example of the change in the behaviour of a blind cave fish to a moving visual
stimulus is shown in Fig. 1. In Fig. 1A the typical swimming behaviour of a fish 2 h after
release in the test aquarium is illustrated by plotting the angular position of the fish over
time. The spontaneous swimming behaviour of the fish is contrasted to its behaviour
during rotation of the striped cylinder (Fig. 1B). Spontaneously, the fish swam slowly, at
an average velocity of 36.7 degrees s21, during the 1 min period shown in the figure.
During rotation of the cylinder at 80 degrees s21 (Fig. 1B), the fish noticeably increased
its velocity. The fish seemed to follow the movement of a stripe by swimming at a
velocity similar to the rotation velocity of the cylinder. From time to time, when the fish
fell behind one stripe, it continued swimming close to the next one. The average velocity
of the fish (during the 1 min recording period shown in the figure) was 69.7 degrees s21,
which is an increase of about 90 % compared to spontaneous swimming.
Fig. 2A illustrates the results of a series of experiments in which the striped cylinder
was rotated at different speeds. The spontaneous ‘cruising’ velocity of the fish in these
experiments was between 40 and 50 degrees s21 (open symbols; means of five animals ±
S.E.M.). If the bar cylinder was rotated at velocities of 20 or 40 degrees s21, which are
lower or similar to the cruising speed of the fish, there was no change in the fish’s
swimming behaviour. The average velocity of the fish during rotation in both cases was
increased only by about 3 degrees s21 compared with spontaneous swimming, and this is
Visual behaviour of blind cave fish
80
80
**
A
B
**
*
**
*
Position (degrees s−1)
93
60
60
40
40
20
**
20
20
40
60
80
100
Bar velocity (degrees s−1)
Stand
Eyes Cont
removed
Rand
Fig. 2. Characteristics of the optomotor response in blind cave fish. (A) Mean velocity (means
of five fish ± S.E.M.) during spontaneous swimming (open symbols) and during rotation of the
cylinder (filled symbols) at different velocities. Asterisks indicate statistically significant
differences (paired t-test; **P<0.05; ***P<0.01). (B) Vestigial eye structures do not mediate
the response. Extirpation of the optic cysts (Eyes removed) does not affect the behaviour of the
fish during rotation of the striped cylinder (N=3). Compare data with those of experiments
using normal fish, carried out according to the standard protocol (Stand; data taken from
Fig. 2A, plotted for comparison). Cont, results of control experiments to test for unspecific
effects, in which the electric motor was turned on but the striped cylinder was not turning.
Rand, additional controls, in which the fish were stimulated with random light flashes
delivered by a circular array of flashing lights.
not a significant increase (20 degrees s21 rotation velocity: P=0.5; 40 degrees s21:
P=0.45).
Rotation of the cylinder at velocities exceeding the cruising speed of the fishes
prompted them to increase their swimming velocities. As shown in Fig. 2A, at drum
velocities of 60 and 80 degrees s21, the velocities of the fish increased from the
spontaneous level to levels that were considerably higher than the cruising speeds
(asterisks indicate statistically significant differences). During rotation at 60 degrees s21,
the fish significantly increased their velocities from a mean cruising speed of 44.4 degrees s21
to a mean velocity of 59.4 degrees s21 (P<0.01), which is very similar to the rotation
velocity of the cylinder. At 80 degrees s21, the mean velocity of the fish was
72.2 degrees s21, a significant increase from cruising speed (P<0.05); (one fish swam at
79 degrees s21, three swam at 70 degrees s21, and one swam at 65 degrees s21). At
100 degrees s21 the mean velocity of the fish was 50.6 degrees s21, which is not
significantly different from that during spontaneous swimming (P=0.3). Inspections of
the video recordings, however, indicated that even at 100 degrees s21, the fish
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T. TEYKE AND S. SCHAERER
occasionally tried to follow the stripes, but managed to do so only for a short period and
then continued swimming at low speeds.
In the majority of cases, the fish followed the movement of the stripes, i.e. they swam in
the turning direction of the cylinder. At the onset of the movement, the likelihood of fish
swimming in the turning direction was about the same as swimming against it (turning
direction: 46 % with versus 54 % against). Thus, we hypothesized that a considerable
number of fish should change their direction in order to follow the movement of the
cylinder. In our combined experiments, 65 % of the fish that were swimming against the
turning direction reversed their swimming direction within the first 15 s of cylinder
movement. In contrast, fish that were swimming in the turning direction continued in
80 % of the cases. In general, we observed an increased propensity of the fish to turn
during rotation of the cylinder. Within the initial 15 s of cylinder rotation, 55 % of the fish
executed a turn, as opposed to only 16 % during control recordings. A recurring
observation was that fish, even though they were swimming in the turning direction of the
cylinder, reversed their swimming direction and swam – for a short period – against the
turning direction of the cylinder. Episodes of swimming in the turning direction
alternated with those of swimming against the turning direction. In a few experiments
(7/180), the fish swam against the turning direction for the entire recording period.
Contrary to our expectations (considering the relative movement of fish and cylinder), the
fish appeared to swim at similar velocities in both directions. One should expect that
swimming against the turning direction should lead to lower velocities, as the fish attempt
to counteract the increase in the rate of the stimulus. We examined this observation more
closely by calculating the velocities separately for the two swimming directions. We
found that the velocities of the fish during rotation of the bars was increased, for both
directions, from that during spontaneous swimming. In one experiment in which a fish
swam exclusively in the counter direction, it also increased its velocity to
60.3 degrees s21, which was very close to the 60 ˚ turning velocity of the cylinder.
Removal of optic cysts does not affect the response
The functional role of the eyes in blind cave fish is controversial, and it is conceivable
that the eyes may be responsible for (or at least contribute to) the detection of the visual
stimulus. To test this possibility, we surgically removed the optic cysts in three fish.
Observations of the lesioned fish revealed that they behave in a way indistinguishable
from intact fish (see also Kähling, 1961). Moreover, when tested according to the
standard protocol (Fig. 2B), the ‘eyeless’ fish increased their velocity from their
spontaneous cruising speed of 40 degrees s21 to above 60 degrees s21 during rotation of
the cylinder (P<0.05). During both spontaneous swimming and rotation of the cylinder,
the ‘eyeless’ fish swam at velocities comparable to those of normal fish recorded under
standard conditions (P=0.7; standard: 60 degrees s21 rotation velocity; 3000 lx
illumination; 2 cm wide stripes; data taken from Fig. 2A). This indicates that
photoreceptors, other than those located in the eyes, may be responsible for eliciting the
optomotor response. Furthermore, preliminary experiments in which the cylinder was
illuminated with either blue or red light indicated that fish are considerably more sensitive
to red illumination. This supports a role for EOPs in eliciting the response, since it has
Visual behaviour of blind cave fish
95
been shown that red light penetrates deeper into the tissue than blue light (see Hartwig
and van Veen, 1979) and thus red light more efficiently stimulates photoreceptors
embedded deep in the tissue. We have obtained two independent lines of evidence which
indicate that extra-ocular photoreceptors and not the eyes are responsible for mediating
the optomotor response in blind cave fish: (1) the unchanged response of the fish after
extirpation of the eyes; and (2) the higher sensitivity of fish to red light than to blue light.
Limiting stimulus conditions of optomotor response
The following experiments address the effectiveness and the limiting conditions of the
visual stimulus in eliciting an optomotor response.
Control experiments
To test for unspecific effects, such as the sound stimulus from the motor during rotation
of the cylinder, we performed two series of control recordings, interspersed among the
regular set of experiments. In control recordings in which the cylinder did not turn (the
electric motor was turned on but the cylinder was not connected to the axle), the fish did
not increase their velocity. As shown in Fig. 2B, in the control experiments (Cont), the
velocity of the fish was found to be very similar to that during spontaneous swimming
(P=0.3), which contrasts with the behaviour recorded under standard conditions (Stand:
the cylinder was rotating; data taken from Fig. 2A).
Random light stimulus
To examine further whether the response of the fish is caused by the movement of the
stripes, as opposed to an unspecific response to stimulation with light, we challenged the
fish with a random pattern of flashing lights. Fifteen lights flashed (approximately 1 s
on/off cycle) independently behind a diffusor to generate a stimulus situation with spatial
characteristics similar to those of the striped cylinder (at an increased contrast).
Stimulating the fish with random light flashes (Fig. 2B, Rand) did not promote a change
in swimming behaviour and the average swimming velocity was very similar to that
during spontaneous swimming (38.1 degrees s21 versus 39.4 degrees s21; P=0.66).
Based upon the two experiments outlined above, we conclude that the increase in
velocity of the fish is a response specifically evoked by the movement of the visual
stimulus.
Intensity of illumination
To evaluate the sensitivity of the sensory system responsible for the detection of the
visual stimulus, we reduced the intensity of the light that illuminated the striped cylinder
by using neutral grey filters. Bar width was 2 cm and the turning velocity of the cylinder
was 60 degrees s21. As shown in Fig. 3A, under high-intensity illumination of 3000, 1000
and 125 lx, the fish significantly increased their velocities above the spontaneous
swimming velocity and closely matched the turning velocity of the cylinder (asterisks
indicate statistically significant differences). At intensities of 20 lx, the fish still
responded to the rotating bars with a slight increase in their velocity, and the increase
from the spontaneous level was significant at the 90 % level. At intensities below 2 lx,
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T. TEYKE AND S. SCHAERER
80
80
B
Fish velocity (degrees s−1)
A
** **
**
**
*
**
*
60
60
**
*
*
40
40
20
20
4
3
2
1
0
log light intensity
50
10
5
Stimulus width (% of cycle)
0
Fig. 3. Limiting conditions of the optomotor response. (A) Average swimming velocity of the
fish under different lightness conditions. As in Fig. 2, the spontaneous swimming velocity
(open symbols; N=5; means ± S.E.M.) is contrasted with that during rotation of the cylinder
(filled symbols). Asterisks indicate statistically significant differences (paired t-test; *P<0.1;
**P<0.05; ***P<0.01). (B) Swimming velocity of the fish under constant lighting conditions
during rotation of cylinders with white stripes of different widths. The stimulus width (the
duty cycle of the stimulus) is given as a percentage of the total cycle.
rotation of the bars did not lead to a significant increase in the velocity of the fish (2 lx,
P>0.25; 0.3 lx, P>0.1). Statistical analysis indicated a significant overall effect of the
intensity of the illumination on the velocity of the fish during rotation of the drum
(ANOVA; P<0.03). The spontaneous velocities did not differ between the experimental
groups (ANOVA; P=0.89).
Spatial resolution
To determine the acuity of the sensory system, we kept the number of stripes the same
(15) and reduced the width of the stimulus (i.e. we decreased the duty cycle by shortening
the white period and increasing the dark period). Fig. 3B shows that the fish responded
reliably when the stimulus width was reduced to 10 %, 5 % and 2 % of the total cycle,
which correspond to subtended visual angles of 4 ˚, 2.2 ˚ and 1.2 ˚, respectively. Reducing
the width of the stimulus to 1 % of the cycle (0.5 ˚ subtended angle) caused a slight, but
insignificant, increase in the fish’s velocity (P>0.1), indicating that the threshold of the
resolution of the sensory system is at stimulus widths subtending an angle of about 1 ˚.
Blind cave fish perform the optomotor response only in certain environments
The blind cave fish responded readily to the moving visual stimulus in the circular
aquarium. Since a previous report has emphasized the importance of spatial features of
Visual behaviour of blind cave fish
97
Fish velocity (degrees s−1)
80
*
*
*
60
*
40
20
Fig. 4. Responses of the fish to the moving stimulus in aquaria of different shapes. Left panel
shows the response of the fish in standard experiments (round aquarium; 60 degrees s21
rotation; data taken from Fig. 2A). Next to the left, the data for fish in a round aquarium
equipped with three 1 cm bars attached to the sides of the aquarium are shown (see schematic
illustration). Next panel shows results of experiments in a round aquarium with a small
cylinder placed in the centre. Right panel depicts the results of experiments in an aquarium of
a shape illustrated in the figure. Note that the fish did not increase their swimming velocities in
aquaria with structured environments. Spontaneous swimming velocities, open symbols;
velocities during rotation of the cylinder, filled symbols. *P<0.1; ***P<0.01.
the environment as determinants of the behaviour of blind cave fish (Teyke, 1989), we
used aquaria of different shapes and tested the response. As shown in Fig. 4, provision of
the round aquarium with three 1 cm bars glued to the side wall of the aquarium (see
schematic drawing in Fig. 4) almost completely eliminated the responses of the fish to the
visual stimulus. Upon rotation of the cylinder, the fish increased their velocities only by
5 degrees s21 above the spontaneous level, which is not a significant increase (P=0.3).
When the circular aquarium was equipped with a small cylinder placed in the centre (see
schematic drawings in Fig. 4), the mean velocity of the fish during spontaneous
swimming was 40 degrees s21 compared with 48 degrees s21 during rotation of the
cylinder. This increase – even though significant at the 90 % level (P<0.1) – is far from
the 60 degrees s21 swimming velocity of the fish usually observed in the round aquarium
during rotation of the cylinder. Experiments in which the shape of the aquarium was
further modified led to more striking results. In an aquarium in which a portion of the
ground area was sectioned off (see schematic illustration of the shape of the aquarium in
the right column in Fig. 4), the mean velocity of the fish during rotation of the cylinder
was 39.6 degrees s21, which is very similar to the 37.4 degrees s21 measured during
spontaneous swimming (P=0.67).
The finding that the shape of the aquarium determines whether the optomotor response
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T. TEYKE AND S. SCHAERER
occurs indicates that spatial features of the environment can override the visually evoked
behaviour in blind cave fish.
Discussion
We have shown that blind cave fish, which supposedly have very limited or no visual
potential, reliably increase their velocity in response to rotation of a striped cylinder, i.e.
they perform an optomotor response. There are several constraints that determine whether
the response can be observed, which might explain why it has been overlooked (e.g.
Voneida and Sligar, 1976). First, if a fish is tested during its initial exploration phase in a
novel environment, the response is more difficult to observe, since the fish’s high velocity
during exploratory swimming does not differ much from that during rotation of the
cylinder. Furthermore, the stimulus velocity (rotation velocity of the striped cylinder) has to
be within a certain window – it must exceed the spontaneous swimming velocity of the fish
(about 40 degrees s21) and be below a maximum velocity of 100 degrees s21. As further
expected, the intensity of the illumination and the size of the stimulus have to be above
certain threshold values to initiate the response. In addition, we have found that for the
response to occur the experimental aquarium has to be without spatial bearings for the fish.
Strong evidence leads us to believe that the increase in velocity of blind cave fish is an
optomotor response, specifically elicited by the moving visual stimulus, even though we
cannot fully exclude the possibility that it is a visually induced exploration phase. Our
evidence is as follows. First and most importantly, even during exploration, when the fish
swim at increased velocities, the rotating visual stimulus promotes a further increase in
velocity (data not shown). Second, the fish reduce their velocity to the spontaneous level
within the first minute after the cylinder stops turning. On the basis of previous
experiments (Teyke, 1989), one would expect an exploration phase to last considerably
longer. Third, we have found that slow turning velocities of the cylinder, as well as
stimulation with random light flashes, do not initiate the response. Since any change of
the environment leads to renewed exploration, slow stimulus velocities and random lights
should both evoke exploration and thus cause an increase in the fish’s swimming velocity.
As we have shown, the remnants of the eyes are not necessary for the detection of the
visual stimulus. After extirpation of the optic cyst, the responses of the fish to the moving
visual stimulus were indistinguishable from those of control animals. This is in accordance
with previous findings (Kähling, 1961; Voneida and Fish, 1984), which indicated that the
eyes of blind cave fish do not contribute to visually evoked behaviour and thus appear to be
nonfunctional. In various other animals it has been shown that, after removal of the eyes,
visual stimuli remained effective in eliciting certain behaviours. In fish (van Veen et al.
1976; Ronan and Bodznick, 1991; Morita et al. 1992), molluscs (Andresen and Brown,
1982; Nishi and Gotow, 1992), reptiles (Underwood, 1973) and birds (Menaker and
Keatts, 1968; Menaker et al. 1970; Oliver and Bayle, 1982), extra-ocular photoreceptors
located within the brain were found to be responsible for eliciting behaviours as diverse as
changing the colour of the skin to controlling circadian activity. By extending previous
studies, we have now shown for blind Mexican cave fish that extra-ocular photoreceptors –
in the pineal organ or yet unidentified extra-pineal photoreceptors – enable the fish to
Visual behaviour of blind cave fish
99
detect a moving visual stimulus. This capability can be achieved by the receptors in two
ways. The receptors could detect the moving white and dark stripes as a sequence of light
and dark events, prompting the fish to alter its behaviour. Alternatively, some kind of
elementary motion detector could be employed within the receptor system. On the basis of
the results of our current experiments, we cannot distinguish between the two alternatives.
Morphological and additional behavioural studies are scheduled to address this issue.
Regardless of how the fish accomplish the detection of the moving stimulus, to our
knowledge this is the first demonstration of motion detection with a visual system other
than the eyes, thus adding another topic to the variety of behaviours elicited by EOPs.
Another key finding of this paper is that blind cave fish respond to moving visual
stimuli only in certain environments. This complements previous findings that the
structure of the environment influences the exploratory behaviour of the fish (Teyke,
1989) and supports the role of the environment as a crucial determinant of behaviour. The
results of our current experiments can be explained by postulating that visual stimuli are
of minor relevance for orientation when other kinds of information about the environment
– such as input from the lateral line system, for example – are available. When a point of
reference in the environment provides spatial cues for orientation (such as the three bars
or the sectioned off aquarium; see schematic drawing of the shapes of the aquaria used in
Fig. 4), the fish do not respond to the visual stimulus. One can speculate that the position
of the objects provides the fish with unequivocal information that the environment has not
changed and, therefore, they do not respond to the visual stimulus. In contrast, the round
aquarium, and to a lesser degree the round aquarium with a cylinder in the centre,
provides no point of reference for the fish’s orientation. Under these circumstances, the
moving visual stimulus might indicate that the environment is changing and prompt the
fish to respond accordingly. In other words, when the fish have access to spatial bearings
within the aquarium from other sensory systems, the moving visual stimulus does not
cause an optomotor response. If, however, the fish are deprived of other environmental
cues for orientation, they do respond to the moving visual stimulus. These findings
indicate that the response of blind cave fish to moving visual stimuli is directly associated
with knowledge of the stability of the environment.
The optomotor response has mostly been employed to study motion detection in
animals, and a variety of characteristics of the response and the underlying movement
detectors have been worked out (see, for example, Borst and Egelhaaf, 1989). In our
study, we have employed a typical optomotor response stimulus paradigm but our
experiments connote a functionally different response. This difference became apparent
in the experiments in which different environments were employed and concerns the
behavioural relevance of the response. We have therefore deliberately abstained from
analyzing our data according to the established premises. Our results suggest that the
behaviour elicited by the moving stimulus is specifically adapted to cope with changes in
the environment, which fish might experience when drifting in currents, for example. A
mechanism to counteract these environmental changes can encompass a group of
different behaviours, and it is not imperative that these behaviours be coupled to the
moving stimulus (i.e. these behaviours do not necessarily have to comply with previous
findings regarding the optomotor response, such as a close coupling between the pattern
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movements and the evoked movements of the animals). We hypothesize that a fish can
engage in several different behaviours to counteract changes in its environment brought
about by a moving stimulus. One of these behaviours might be to swim at a velocity
which corresponds to that of the stimulus. It is also conceivable that, in some cases, the
fish might continue to swim against the turning direction.
We would like to extend our conclusion to other fish by suggesting that at least some of
the responses observed and described under the umbrella of optomotor responses conform
more closely to the category of behaviour that we have described. It has been reported that
frogs and newts stopped responding to the moving visual stimulus as soon as they were
able to establish tactile contact with the walls of the tank (Birukow, 1950). In addition,
comparative studies on fish showed that bottom-dwelling fish do not perform optomotor
behaviour (Harden Jones, 1963; see also Arnold, 1974). These findings can be explained
by our hypothesis: bottom-dwelling fish maintain contact with the substratum and thus
have access to tactile cues which can be used as tell-tale signs that the environment has not
changed. Similarly, frogs and newts perform optokinetic behaviour when they are
swimming freely in a tank, but as soon as they establish tactile contact with the walls (i.e.
they have acquired a point of reference in their environment), they cease to respond.
This notion is further supported by our recent studies on goldfish in which two
competing stimuli were delivered, one in the nearfield and one ‘environmental’ stimulus
at a distance (Teyke and Schaerer, 1993). We found that stimuli moving at a distance
override stationary proximate stimuli and effectively initiate an optomotor response.
And, vice versa, stationary stimuli at a greater distance reduce or abolish the response to
moving stimuli close to the fish. These findings support the hypothesis that the
environment per se is the critical determinant for the response to occur.
Our notion suggests that information about the environment, which can be acquired via
different interacting sensory systems and can be differentially weighted, determines
whether the fish respond to a moving stimulus. We further propose that the optomotor
response consists of various behavioural strategies developed by the animals to offset the
changes in their environment.
We would like to thank Drs C. Neumeyer and C. von Campenhausen for comments on
an earlier draft of this manuscript.
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