/ . Embryol. exp. Morph. Vol. 72, pp. 19-37, 1982
Printed in Great Britain © Company of Biologists Limited 1982
19
The retinotectal fibre pathways from normal
and compound eyes in Xenopus
By J. W. FAWCETT 1 AND R. M. GAZE 1
From the National Institute for Medical Research, London
SUMMARY
Horseradish peroxidase was used to demonstrate the nature of the retinotectal fibre
pathways from normal eyes and from compound double nasal (NN), double temporal (TT)
and double ventral (VV) eyes in Xenopus. From normal eyes, nasal fibres were widespread
in the optic tract and mostly entered the tectum through the medial and lateral brachia.
Ventral retinal fibres approached the tectum via the medial brachium and dorsal retinal
fibres passed through the lateral brachium, while temporal retinal fibres formed a narrow
band in the centre of the tract and entered the tectum directly at its rostral border.
Fibres from NN eyes formed a wide tract and strong medial and lateral brachia. Fibres
from VV eyes all entered the tectum via the medial brachium andfibresfrom TT eyes formed
a narrow tract and entered the tectum directly from its rostral extremity. Thus fibres from
each type of compound eye followed pathways to the tectum that were appropriate to the
embryonic origin of the retina forming the compound eye.
INTRODUCTION
In amphibians and fishes the optic tectum is the main site of termination of
optic nerve fibres. The optic nerve terminals are distributed in such a way as to
provide a continuous map of the retina across the surface of the tectum. The
nature of this map has been known for many years from behavioural (Sperry,
1944), histological (Attardi & Sperry, 1963) and electrophysiological (Gaze &
Jacobson, 1963) evidence. It has also been known for many years that the
fibres of the retinotectal projection may regenerate when cut and restore the
orderly map that existed previously (Sperry, 1944; Gaze & Jacobson, 1963).
One of the most fruitful approaches to understanding the mechanisms by
which the retinotectal projection is formed has been the size-disparity experiment (Attardi & Sperry, 1963). In the study of development, as opposed to
regeneration, this has usually been achieved by investigating the connexions
made by fibres from 'compound eyes'. These compound eyes are formed in
Xenopus by the surgical apposition of two half-eyes in one orbit at an embryonic
stage (e.g. stage 32 of Nieuwkoop & Faber, 1956) before the developing eye
connects with the developing brain. One can in this way construct an eye out of
1
Authors' address: National Institute for Medical Research, The Ridgeway, Mill Hill,
London, NW7 1AA, U.K.
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J. W. FAWCETT AND R. M. GAZE
two nasal halves (NN), two temporal halves (TT) or two ventral halves (VV),
thus presenting the brain with a normal number of optic fibres but only half
the normal complement of retinal positions. It is then possible to study later
the way fibres from the compound eye project to the tectum (Gaze, Jacobson &
Szekely, 1963; Straznicky, Gaze & Keating, 1974).
When TT and VV eyes first establish connexions with the tectum, they
restrict their terminal arborizations to rostrolateral tectum (TT eyes) or medial
tectum (VV eyes) whereas NN eyes from the start appear to innervate all the
available tectum except for a highly localized region in the most rostral part
(Straznicky, Gaze & Keating, 1981). In later life neuropil from all three types of
eye covers the tectum completely (Gaze et al. 1963; Straznicky et al. 1974) and
the electrophysiological maps demonstrate that each (similar) half of the
compound eye spreads its connexions across the whole tectum in proper order
and orientation.
Fibres from a VV eye restrict themselves, during development, to the medial
brachium of the optic tract (Straznicky, Gaze & Horder, 1979; Steedman,
1981). This finding, together with other recent studies on developing and regenerating projections from compound eyes, suggests that the role of fibre organization in the optic tract may be very important in the establishment of the retinotectal projection map (Straznicky et al. 1981).
In the past three years methods have become available for the study of optic
fibre pathways in histologically cleared, whole-mounted brains in young amphibians (Steedman, Stirling & Gaze, 1979; Fujisawa, Watanabe, Tani & Ibata,
1981). In this paper we describe the retinotectal projections in normal Xenopus
and in animals with a compound NN, TT or VV eye, using a whole-mount
Horseradish Peroxidase (HRP) method to demonstrate both the extent of the
tectal coverage and the nature of the organization in the optic tract. In a
following paper (Gaze & Fawcett, in preparation) we show what happens to these
aspects of the retinotectal projection when fibres are allowed to regenerate from
a normal eye to both tecta and from a compound eye to both tecta when the
ipsilateral tectum is either normally innervated or 'virgin' (i.e. previously
uninnervated by retinotectal fibres).
METHODS
Embryonic operations
Adult Xenopus were induced to breed by injections of Chorionic Gonadotrophin, 400 units to the female, 200 units to the male.
Operations were performed in full-strength Niu Twitty solution containing
0005 % MS 222 (Sandoz, tricaine methane sulphonate). The left eyes of embryos
between stages 29 and 30 were operated on to produce compound eyes. To make
an NN eye, the nasal half of a donor right eye was removed and used to replace
the temporal half of the host left eye (see Fig. 1). TT and VV eyes were made in
Xenopus retinotectal pathways
21
Fig. 1. Operation to construct a double-nasal compound eye.
comparable fashion. Some host animals also had their right eye removed at the
same time. After operation the embryos were left in full-strength Niu Twitty
for about 30 min, then transferred to 1/10 strength Niu Twitty.
Rearing
Animals were reared in 1/10 strength Niu Twitty. Until metamorphosis they
were fed on Boots liver and vegetable baby food, and after metamorphosis on
Tubifex.
Electrophysiological mapping
Animals were anaesthetized with MS222, their optic tecta were exposed, and
then they were mounted at the centre of a perspex globe filled with oxygenated
Niu Twitty solution containing 1:10000 MS222. This was placed at the centre
of an Aimark perimeter, with the compound eye centred, and the other eye, if
any, covered.
Visually evoked potentials were elicited by movement of a black disc in the
visual field, and recorded through a glass-insulated tungsten electrode with a
tip size of around 20 jam. Usually only 9 points were recorded from the tectum,
but this was quite adequate to demonstrate whether or not the animal had the
expected compound eye projection. Those that did not were discarded.
Application ofHRP
The eye was removed under anaesthesia, the optic nerve being cut near to the
back of the eye. When haemostasis was achieved, crystalline HRP (Sigma
type 6) was applied to the optic nerve stump. Animals were then left with their
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J. W. FAWCETT AND R. M. GAZE
heads out of water for a further 20 min. In some animals HRP was applied by
needle to a localized region of retina.
Histology
Twenty-four hours after HRP application the animals were anaesthetized,
then killed by perfusion with 0-25 M-sucrose followed by 2-5 % glutaraldehyde
in 0-1 M-phosphate buffer at pH 7-2. The brains were removed and transferred
to cold fixative for a further hour, during which time the pia mater was stripped
away.
The brains were then reacted to visualize the HRP, using the method of
Adams (1977) modified in this laboratory by R. V. Stirling.
After fixation the brains were washed for 10 min in phosphate buffer, then for
1 h in 0-1 M-Tris buffer at pH 7-2. They were then transferred to 1 % cobaltous
chloride in Tris for 1 h, then washed in Tris for 10 min, and in two changes of
phosphate buffer for 10 min each. They were then put in phosphate buffer
containing 50 mg/100 ml of diamino benzidine and 1 % DMSO for 90 min.
Meanwhile more of the DAB solution was cooled on ice. At the end of the
90 min, 4 ml /100 ml of 0-3 % H2O2 was added, and the brains transferred to
this cooled solution. Incubation was now continued until the optic fibres were
sufficiently densely stained, usually about 20 min. The preparations were now
washed in phosphate buffer, dehydrated in alcohols, and cleared in methyl
salicylate.
Successful preparations were drawn using a camera lucida. The whole-mount
method used in the experiments reveals very well the optic fibres lying fairly
superficially in the brain but does not show deep fibres.
RESULTS
Projections from normal eyes
When the nerve from a normal eye is labelled with HRP, the fibres in the
optic tract contralateral to the eye are seen to be compactly arranged (Fig. 2).
Under the dissecting microscope at magnifications of up to 50 x , the fibres
appear mostly to run parallel to each other with little crossing of one fibre by
another and with the whole tract gently fanning out as it approaches the tectum. The edges of the tract are regular and well defined. Fibres running from
the eye up the ipsilateral tract are few and appear to terminate mainly in the
neuropil of Bellonci and the pretectal neuropil.
The contralateral tectum is uniformly and completely covered by labelled
neuropil. Other target areas of the optic fibres are also seen, such as the pretectal
neuropil, the neuropil of Bellonci and the basal optic neuropil (Fig. 2). As
optic fibres approach the tectum they form medial and lateral brachia while
some fibres enter the tectum directly at its rostrolateral extremity. In most
Xenopus retinotectal pathways
(a)
(c)
Fig. 2 (a) Dorsolateral photograph of a whole-mount preparation showing the optic
pathways in a normal young Xenopus. The right optic tract is seen coming up
round the diencephalon to the tectum. Rostral is to the right. The projection of the
neuropil of Bellonci beyond the medial edge of the tract is misleading; retinotectal
fibres do run as far medial as this but do not show up in this low-power photograph.
(b) Diagram of a dorsal view of the fibre projection from the left eye to the right tectum in another normal Xenopus just after metamorphosis. This and the other
projection drawings shown are camera-lucida drawings of preparations in which the
optic nerve (or a part of the retina) had been labelled with HRP. Areas of labelled
neuropil are indicated by stipple, (c) Dorsolateral view of the same preparation.
Bar = 1 mm for b and c.
23
24
J. W. FAWCETT AND R. M. GAZE
v
y
,3-
Xenopus retinotectal pathways
25
cases the medial brachium is much more obvious than the lateral brachium,
which may consist of a few fibres only. Brachial fibres may almost completely
encircle the tectal neuropil, leaving a region at the caudal end of the tectum
devoid of circumferentially running fibres.
The retinotopic nature of the tectal distribution of the optic fibres is well
shown when small groups of fibres from localized regions of the retina are
labelled with HRP (Fig. 3).
Fibres from nasal retina are distributed across the entire width of the tract
as they climb up around the wall of the diencephalon, but as they approach the
tectum they diverge into two brachia, leaving a small triangular area in the
middle of the tract at the tectodiencephalic junction which is relatively deficient
in fibres (Fig. 4a). A few fibres enter directly onto the tectum and take devious
paths across it (Fig. 4b). In all cases the nasal fibres, whether they pass around
the tectum in one or other brachium or whether they cross the tectum from the
front, form their terminal neuropil caudomedially.
Fibres from ventral retina reach their tectal destination via the medial branch
of the optic tract (Fig. 5). They form terminal neuropil in medial and rostromedial tectum. The rest of the tectum shows no optic neuropil and there are
no labelled fibres to be seen in the lateral brachium of the tract.
Fibres from dorsal retina approach the tectum via the lateral brachium and
form their terminal neuropil in lateral tectum (Fig. 6 a). When the labelled
tectal neuropil extends far caudally and thus indicates that nasodorsal retinal
fibres were also filled, several fibres are to be seen passing around the tectum
in the medial brachium to reach caudal tectal regions (Fig. 6 b).
Fibres from temporal retina form a coherent bundle centrally placed between
the medial and lateral edges of the tract (Fig. 7). They enter onto the tectum
directly and form terminal neuropil rostrolaterally.
Fig. 3. Photographs of whole-mount preparations from retinal part-fills, (a) Temporal/ill. Fibres from temporal retina form a narrow band passing up the middle of
the region normally occupied by the tract. The fibres enter directly onto the rostral
tectum and terminate there. This preparation is also illustrated in Fig. 7. (b) Nasal
fill. Fibres from nasal retina are distributed across the entire width of the optic
tract. They mostly diverge into medial and lateral brachia at the rostral tectal
margin. Fibres then run right round the tectum (some fibres, not visible in this
photograph, cross the tectum from the front) to terminate caudomedially. This
preparation is also illustrated in Fig. 4. In this animal the preparation was of the
left tract and tectum. This has been photographically reversed here to facilitate
comparison with the other photographs shown, (c) Ventral fill. Fibres from
ventral retina form a tract of practically normal width, except near the tectum,
where the lateral part of the tract is missing. All fibres enter the tectum via the
medial brachium of the tract and distribute themselves across rostromedial tectum.
This preparation is also illustrated in Fig. 5. (d) Dorsal fill. Fibres from dorsal
retina pass via the lateral brachium and terminate in lateral tectum. This preparation
is also illustrated in Fig. 6a.
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J. W. FAWCETT AND R. M. GAZE
(a)
(b)
Fig. 4. (a) Drawing of a dorsolateral view of a preparation from a normal animal
in which nasal retinal fibres (from the right eye) had been labelled with HRP.
Terminal neuropil on the tectum is restricted to caudomedial regions and the rest of
the tectum is empty. The neuropil of Bellonci is labelled in the diencephalon. In
this low-power view all the labelled fibres appear to run in either the medial or the
lateral brachium. A fewfibreswhich cross the tectum to reach the terminal neuropil,
not seen here, may be seen in the higher power view shown in b. Bar = 1 mm. {b)
Higher magnification of the same tectum, to show the fibres which wander across
the tectum from the rostral edge to reach the terminal neuropil caudomedially.
Bar = 250 fim.
Xenopus retinotectal pathways
(a)
(b)
Fig. 5. (a) Dorsal view of a preparation from a normal animal in which ventral
retinal fibres (left eye) had been labelled with HRP. Terminal neuropil is confined
to rostromedial tectum. Neuropil is also seen in the pretectal region on both sides.
Bar = 1 mm. (b) Dorsolateral view of the same preparation. All the fibres going
to the tectum run in the medial brachium. Labelled fibres are also seen in the
basal optic tract, leading to the basal optic neuropil. Magnification as in (a).
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J. W. FAWCETT AND R. M. GAZE
(a)
(b)
Fig. 6. (a) Dorsolateral view of a preparation from a normal animal in which dorsal
retinal fibres (left eye) had been labelled with HRP. All fibres enter via the lateral
brachium to reach their regions of terminal neuropil in lateral tectum. (6) Dorsolateral view of a preparation from a normal animal in which dorsal retinal fibres
(left eye) had been labelled with HRP. In this preparation the fill included more
nasal fibres than the previous figure. Labelled fibres can be seen running in the
medial brachium, and across the tectum, to reach the region of terminal neuropil,
which here extends into caudal tectum. Bar = 1 mm for (a) and (b).
Xenopus retinotectal pathways
29
Fig. 7. Dorsolateral view of a preparation from a normal animal in which temporal
retinal fibres (left eye) had been labelled with HRP. The fibres in the tract form a
compact bundle which heads straight for the terminal zone in rostrolateral tectum.
Bar = 1 mm.
Projections from compound eyes
NN eyes
Fibres from an NN eye form an optic tract that is wider than normal (Fig. 8).
The fibres are well aligned with each other and the tract has well-defined edges.
As they approach the tectum the fibres tend to concentrate in two brachia
between which there is, in many cases, a triangular region relatively devoid of
fibres. The terminal neuropil formed by NN fibres covers the entire tectum
uniformly.
TT eyes
The optic tract from a TT eye tends to be narrow in comparison with a normal
tract (Fig. 9). Fibres are concentrated in the middle region of the tract and the
tract thins out markedly at its edges, particularly its medial edge, which consists of a very few fibres rather widely spread. Fibres run parallel in the tract
and the edges of the tract are well aligned although poorly demarcated.
Fibres approach their tectal destination directly and there is very little brachium formation. In particular, the medial brachium, which in normal animals is
more obvious than the lateral brachium, is not seen in projections from TT
eyes. The lateral fibres in Fig. 9 b are heading for lateral tectum which is rather
far caudal for a TT projection, and this suggests that the projection had a large
component of dorsal fibres; in other cases neither medial nor lateral brachia
were seen (Fig. 10). Fibres from TT eyes form terminal neuropil which is
restricted (in these animals, shortly after metamorphosis) to rostrolateral
tectum.
2
EMB 72
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J. W. FAWCETT AND R. M. GAZE
(c)
Fig. 8. (a) Dorsal view of the projection from an NN eye. Bar = 1 mm. (b) Dorsolateral view of the same preparation. The tract is heavy and wide, with massively
constructed brachia. Tectal coverage is complete. Bar = 1 mm. (c) The visuotectal projection map from this animal. The tectal diagram (top) shows three rows
of recording positions, indicated by numbers and filled circles. The open arrow
points rostrally along the midline. The chart of the visual field (bottom) indicates
optimal stimulus positions corresponding to each tectal recording position. The
distribution of positions in the visualfieldis reduplicated about the vertical meridian
in the fashion characteristic of NN eyes. N, nasal; S, superior; T, temporal;
I, inferior.
Xenopus retinotectal pathways
31
VV eyes
Fibres from VV eyes form an optic tract that is of approximately normal
width. The fibres in it run parallel to one another and the edges of the tract are
well denned. As the fibres approach the tectum they all veer into the medial
brachium, which tends to be large (Fig. 11). The region of the lateral brachium
is conspicuously empty and this gives a remarkable appearance since the lateral
part of the tectum, which contains labelled neuropil, juts out from the tract at
an acute angle. The terminal neuropil formed by VV fibres is most dense (in
these animals, shortly after metamorphosis) over the rostral half or two-thirds
of the tectum.
DISCUSSION
The results presented in this paper confirm reports (Steedman, 1981) that
fibres from different regions of the Xenopus retina travel in particular parts of
the optic tract. As they approach the tectum fibres from ventral retina travel in
the medial brachium of the tract, fibres from dorsal retina travel laterally
in the tract and temporal retinal fibres are concentrated towards the middle of
the tract, while nasal retinal fibres are widespread. Thus ventral fibres use the
medial brachium, dorsal fibres the lateral brachium and temporal fibres use
neither brachium but pass straight on to rostral tectum. Nasal fibres use all
routes to reach their terminal regions on the tectum; most use medial or lateral
brachium but a few pass right across the top of the tectum to reach their caudal
destination. With the exception of those few nasal fibres, all retinal fibres enter
the tectum adjacent to their eventual areas of termination.
Our results also confirm that, near the tectum, fibres from compound eyes
travel only in the part of the optic tract that would be occupied by fibres from
equivalent areas of normal eyes. These findings bring up two main questions
of interest: how do fibres come to grow along these specific pathways? And
what relevance does this have to the establishment of an ordered retinotectal
map?
Our results require a mechanism that actively patterns fibres into specific
pathways according to the embryonic positions of origin of the areas of retina
from which they come. Any mechanism dependent on the maintenance of
neighbour relations between fibres all the way from eye to tectum is inadequate
to explain these results. In the case of a normal eye, it is possible to conceive that
fibres occupy their observed positions in the mediolateral dimension of the
optic tract near the tectum simply by maintaining their neighbour relations.
However, there is now direct evidence that fibres lose contact with their original
neighbours in the first part of the optic pathway (Fawcett, 1981; Fawcett, Gaze,
Grant & Hirst, in preparation). Moreover, if fibres from a compound eye
merely maintained their neighbour relations until they reached the tectum, the
2-2
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J. W. FAWCETT AND R. M. GAZE
(a)
Fig. 9. (a) Dorsal view of the projection from a TT eye. Bar = 1 mm for (a) and (6).
(b) Dorsolateral view of the same preparation. Tectal coverage in this preparation
extends rather far caudal and this is associated with some fibres in the lateral
brachium, not usually to be found in TT preparations, (c) The visuotectal projection map from this animal. The conventions are as in Fig. 8(e). The map is characteristic of those from TT eyes.
Xenopus retinotectal pathways
33
Fig. 10. Dorsolateral view of the projection from another TT eye. In this case the
projection is restricted to more rostrolateral parts of the tectum than in the previous
figure and most fibres in the tract run straight onto the rostrolateral tectum.
Bar = 1 mm.
optic tract from such an eye would look quite normal; fibres from the dorsally
implanted half of a VV eye would grow into the lateral brachium of the tract,
rather than all choosing to crowd into the medial one.
The fibre patterns we have observed could be produced by a mechanism in
which the patterning information was in the tract itself or on the tectum; or
some combination of the two.
The first mechanism would require the tract to carry positional labels of
some sort, so that appropriately labelled retinal fibres would travel in the right
part of the tract. Thus fibres from ventral retina, or retina of ventral embryonic
origin, would only be able to pass through that part of the tract available to
ventral fibres, which, near the tectum, is the medial brachium. A VV eye, for
instance, has no retina of embryonic dorsal origin, and would send out no
fibres capable of growing into the lateral brachium, which would therefore
remain empty.
If the information giving rise to the patterning of the fibre pathways were on
the tectum, one would have to propose that fibres branch extensively before
they reach the tectum, and that those that reach an inappropriate region
degenerate back to the branch point. We observe that fibres grow around the
tectum in brachia, and (except for some nasal fibres) each enters the tectum at a
point adjacent to its termination site. One would thus also have to propose that
the branch point is before the rostral margin of the tectum, and that the branches,
having grown to the tectum via one of the brachia, form a termination immediately at the point at which they first enter the tectum (see Fig. 12).
There are several lines of evidence against this latter type of mechanism:
(a) Two recent studies have provided evidence against fibres from a given
area of retina initially growing to sites all over the tectum. Straznicky et al.
34
J. W. FAWCETT AND R. M. GAZE
(a)
(ft)
Fig. 11. (a) Dorsal view of the projection from a VV eye. Bar = 1 mm for (a) and
(b). (b) Dorsolateral view of the same preparation. In this preparation all fibres
heading for the tectum pass via the medial brachium. (c) The visuotectal projection
map from this animal. The conventions are as in the previous two visuotectal
maps with the exception that here the rows of tectal recording positions run rostrocaudally. In this case the visual field positions show reduplications about the
horizontal axis (which shows a 30° clockwise twist), characteristic of projections
from double ventral eyes.
Xenopus retinotectal pathways
35
Fig. 12. Diagram to illustrate a possible but unlikely mechanism to account for the
results described. A fibre growing from dorsal retina is illustrated. It branches
extensively just rostral to the tectum, sending connexions to all parts of it. All of
these except that to lateral tectum then degenerate. See text.
(1981) found that the initial projection from a compound eye, when assessed
in young larvae, occupied only a limited area of tectum; and Holt (personal
communication) has recently found that at mid 40's stages, when the tectum
first receives optic innervation, this is retinotopically organized.
(b) The projection from a compound eye spreads in time to cover the entire
tectum, but we see no indication that fibres growing to the tectum after this
has happened fill a greater proportion of the optic tract as a result; fibres from
the temporal pole of a VV eye will innervate rostrolateral tectum, but they still
grow there via the medial brachium. The tectal termination of a fibre does not,
therefore, in this instance define its position in the tract.
(c) There is no convincing evidence for the existence of tectal labels that guide
fibres to their termination sites during development. The observed shift of
fibre terminals as the tectum grows (Gaze, Keating, Ostberg & Chung, 1979),
the fact that the compound eye projection spreads to cover the entire tectum,
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J. W. FAWCETT AND R. M. GAZE
and the observation that a normally orientated map can be formed on a tectum
rotated in embryo (Chung & Cooke, 1978) all argue against tectal labels having
an important role in development.
It seems then that pathways in the optic tract are probably only open to
fibres carrying the correct retinal positional labels. How this arises in early
development remains to be shown, but the fact that it is so throughout most of
development means that most fibres are normally fed onto the tectum adjacent
to their regions of termination. This could account for the normal orientation
of the map and for its ordering, at least to a first approximation. The fine details
of the ordering of the map, together with the modifications required to cope with
retinal and tectal growth, could then be achieved by further fibre/fibre interactions, of the sort, for instance, proposed by Fawcett & Willshaw (1982).
A small proportion of the fibres of nasal retinal origin enter the tectum at its
rostral margin, yet still form their terminations on caudal tectum. These fibres
may have initially terminated rostrally, but have since shifted their terminations
as a result of such fibre/fibre interactions on the tectum.
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{Received 21 April 1982, revised 24 May 1982)