/ . Embryol. exp. Morph. Vol. 60, pp. 125-140, 1980
Printed in Great Britain (gl Company of Biologists Limited 1980
125
Regeneration of optic nerve fibres
from a compound eye to both tecta in
Xenopus: evidence relating to the
state of specification of the eye
and the tectum
By R. M. GAZE 1 AND C. STRAZNICKY 2
From the National Institute for Medical Research, London
SUMMARY
Xenopus with one double-nasal (NN). double-temporal (TT) or double-ventral (VV)
eye were induced to regenerate optic fibres from the compound eye to both tecta after
metamorphosis. The extent of the projection from the compound eye was then estimated
autoradiographically at various intervals after nerve section. The regenerated projection
covered the whole of the contralateral tectum but covered only a restricted part of the
ipsilateral tectum; thus NN eyes innervated caudomedial tectum only, TT eyes innervated
rostrolateral tectum only and VV eyes innervated medial tectum only. Since the tectum
ipsilateral to the compound eye also received the projection from the normal eye these
results are taken to indicate that NN, TT and VV eyes are unregulated systems in terms of
the retinal positional markers that they carry; each such eye bears only the appropriate
half-set of such markers.
INTRODUCTION
In normal Xenopus the map of the retina formed by the distribution of optic
nerve fibres on the optic tectum has the following characteristics: (1) it is well
ordered in that neighbourhood relationships on the retina are preserved in the
tectal distribution of optic fibre arborisations, as determined electrophysiologically; (2) it is oriented in a particular way, such that nasal retina projects
caudally on the tectum, temporal retina projects rostrally, ventral retina
projects medially and dorsal retina projects laterally; (3) in post-metamorphic
animals the map covers the entire surface of the tectum; (4) the map is restored
on regeneration of the optic nerve.
Numerous studies on regenerating optic nerves in larval and adult animals
have indicated that the ability of amphibian and fish optic fibres to restore the
1
Author's address: National Institute for Medical Research, Mill Hill, London, NW7 1A A,
U.K.
2
Author's address: Centre for Neuroscience, School of Medicine, Flinders University of
South Australia, Bedford Park, South Australia 5042, Australia.
0
EMB 60
126
R. M. GAZE AND C. STRAZNICKY
original tectal map after section of the nerve is usually controlled by cellular
markers in retina and tectum, and the action of some sort of recognition or
affinity mechanism between them (Attardi & Sperry, 1963; Jacobson & Levine,
1975; Hope, Hammond & Gaze, 1976). We are concerned to find out how
such a retinotectal projection might come about during development, and what
role retinal and tectal cell markers may play in this.
The present paper is one of a series in which we consider the connections
formed by 'compound eyes' in Xenopus. Compound eyes are formed by fusing
two half-eye fragments into one eye blastema in an embryo. Numerous varieties
of compound eye can be made, according to how the eye is subdivided into
fragments, and whether or not the host fragment and the graft fragment are
from the same, or opposite, sides of the head. Here we are concerned only with
conventional double-nasal (NN), double-temporal (TT) and double-ventral (VV)
eyes.
The retinotectal fibre projections from compound eyes are abnormal. With
NN and TT eyes, each (similar) half-eye projects, in proper order, across the
entire tectum in the adult and not just half of it (Gaze, Jacobson & Szekely,
1963); the retinotectal projection is thus reduplicated about the dorsoventral
meridian of the retina. With VV eyes the retinotectal projection is reduplicated
about the horizontal meridian of the retina (Straznicky, Gaze & Keating, 1974)
and, again, each half-retina spreads extensively across the tectum.
We have previously shown that half-eye fragments retain their original
developmental programme relating to map orientation, both when they are
formed into a compound eye (Straznicky & Gaze, 1980; Gaze & Straznicky,
1980) and when they are left as half-eyes, rounded-up in the orbit (Straznicky,
Gaze & Keating, 1980). The fragments comprising a compound eye have also
been shown to retain their proper sequence of histogenesis (Straznicky & Tay,
1977) and, in the case of a VV eye, to form optic fibre pathways characteristic
of the pieces of retina comprising the compound eye (Straznicky, Gaze &
Horder, 1979).
In the present paper we are particularly concerned with the third aspect of
compound-eye projections, mentioned above; that is, tectal coverage. Conventional NN, TT and VV eyes, when recorded in adult life, are found to have
spread their projections from each half-retina across the tectum (Gaze et a/.
1963; Straznicky et al. 1974) and we have recently shown that this also applies
to other varieties of compound eye (Straznicky & Gaze, 1980), in which, as
in conventional NN, TT and VV eyes, the component eye fragments together
make up an eye which is deficient in half the positional values of the normal
eye. If, however, a compound eye is constructed which is complete in terms
of positional values, so that the whole comprises a 'normal' eye but is merely
internally disarranged, each half-retina tends to restrict its projection to its
appropriate half-tectum (Gaze & Straznicky, 1980).
The most widely held view on how retinotectal connections develop involves
Nerve regeneration from compound eyes in Xenopus
127
Sperry's chemoaffinity hypothesis (Sperry, 1943; 1944; 1945; 1951; 1963; 1965).
This supposes that cells in the developing retina acquire place-related cytochemical labels or markers; that cells in the developing tectum independently
acquire a matching set of labels; and that a properly ordered map is established
between retina and tectum by the action of selective chemoaffinity between
labels in the two structures.
The fact that the projection from a normal eye eventually extends across
the entire tectum gives us, however, little insight into the mechanisms that may
be involved. The fact that a conventional NN or TT compound eye behaves
differently may tell us more. The spreading of the projection from each halfretina raises interesting questions such as:
(1) Does each half of such a compound eye contain a complete set of cell
markers rather than a half set? In other words, is the compound eye a regulated
system in terms of its cell specificity labels?
(2) What is the distribution of affinity markers across the tectum connected
to a compound eye?
In a former series of experiments we attempted to answer such questions.
We found that, after uncrossing the chiasma in animals with one compound
eye, the compound eye was able to form a complete and typical reduplicated
map across the whole of the tectum formerly innervated by the normal eye,
while the normal eye could form an approximately normal map across the
tectum formerly innervated by the compound eye (Straznicky, Gaze & Keating,
1971). We concluded that there was considerable and unexpected plasticity in
the way the retinotectal map could be formed. However, we did not, at that
time, appreciate the full significance of some of the maps obtained.
In the light of recent work by Schmidt (1978), showing that optic fibres can
modify tectal positional markers in adult goldfish, we have re-examined the
results of our 1971 series of experiments. We now conclude that the maps, in
particular Figs 7 and 10 of that paper (as well as the remaining, unpublished,
maps from that series) suggest that the markers existing on the compound-eye
tectum were those appropriate to the type of half-eye forming the (previous)
compound-eye projection; and that the normal eye, now innervating this
tectum, was finding it difficult to establish a foothold for fibres from the
'foreign' half-retina.
Thus those experiments, in which six months were allowed to elapse between
uncrossing the chiasma and recording the projection, indicated that the prior
innervation of the tectum by a compound eye caused particular abnormalities
in the map when that tectum was later innervated by a normal eye. Further
investigation was called for and the results are presented in this and the next
paper of this series.
In the present paper we discuss the regeneration of fibres from a compound
eye to both contralateral and ipsilateral tecta. In the 1971 experiments we had
found that section of the chiasma could lead to bilateral regeneration from
9-2
128
R. M. GAZE AND C. STRAZNICKY
both eyes, so that the role of optic fibres in generating and/or modifying the
tectal markers could not be assessed properly. In the experiments reported
here we have used a simpler situation where bilateral regeneration from the
compound eye only had occurred, brought about by section of its nerve just
after metamorphosis (Glastonbury & Straznicky, 1978). We show that where
the compound eye regenerates fibres to its own contralateral tectum the
projection extends across virtually the entire surface. When a compound eye
regenerates fibres to the ipsilateral tectum, which carries also the projection
from the normal eye, the compound-eye projection is restricted to only part of
the tectal surface and the region so innervated is appropriate to the nature of
the compound eye. Thus NN eyes innervate caudo-medial tectum only; TT
eyes innervate rostro-lateral tectum only and VV eyes innervate medial tectum
only.
The results demonstrate unequivocally that these compound eyes are
unregulated systems in that each contains only cell markers appropriate to
a half-eye. And since a compound eye, regenerating fibres to its own contralateral tectum, covers the entire surface, we can also say that the tectal markers
on such a tectum have been positioned (or repositioned) by the fibres themselves.
Some of these results have been published in abstract elsewhere (Gaze &
Straznicky, 1979).
METHODS
Laboratory-bred Xenopus laevis were used in this study. Since the methods
used have been described in a previous paper (Straznicky & Gaze, 1980) only
a short account is given here.
Microsurgery
The right eyes of stage-32/-33 embryos (Nieuwkoop & Faber, 1956) were
operated on in full-strength Niu-Twitty solution to obtain a double-nasal
(NN), double-temporal (TT) or double-ventral (VV) eye. Embryos were
anaesthetized with 0005 % solution of MS222 (Sandoz, tricaine methane
sulphonate) and the temporal half of the eye anlage was substituted by a left
nasal half from another embryo, to form an NN eye. Similarly TT and VV
eyes were formed in other embryos. Two weeks after metamorphosis the right
optic nerve from the compound eye was exposed through the mouth and cut
close to the chiasma, under anaesthesia with MS222. The optic fibre projection
was assessed autoradiographically and in some cases, electrophysiologically,
either 5-6 weeks, or 2^-5 months after the operation. In some animals, before
the nerve was cut, the visuotectal projection from the compound eye was
mapped.
Nerve regeneration from compound eyes in Xenopus
129
Histology
[3H]proline (24 Ci/mmol, Amersham) was injected into the posterior chamber
of the compound eye 24 h before sacrifice. In animals up to 8 weeks of age
5 /*Ci were injected and 10/tCi for older animals. The head of the animal was
fixed in Bouin's solution, the dissected brain was embedded in paraffin, serially
sectioned at 10 ftm and mounted on slides. The slides were coated with Ilford K2
emulsion, exposed at 4 °C for 14 days, developed in Kodak Dektol and counterstained with Harris's haematoxylin. Reconstructions of the brains, based on
camera-lucida drawings of every fifth section, were made to assess the extent
of the projection from the compound eyes.
Electrophysiology
Several animals with NN and TT eyes were recorded before or after section
and regeneration of the right optic nerve.
Animals with regenerated right optic nerve, 5 or 6 months after metamorphosis, were anaesthetized with MS222, decerebrated and immobilized with
01 mg of tubocurarine administered intramuscularly. The tectum was exposed
and photographed and the animal set up in a small Perspex globe filled with
oxygenated anaesthetic solution (approximately 0-01 % MS222) at the centre
of an Aimark projection perimeter with the right, compound, eye centred
and the left eye covered.
Visually evoked action potentials were recorded from pre-determined tectal
positions and the corresponding receptive fields located. The visuotectal
projection from the operated eye was estimated by sampling about 30 tectal
recording points.
For control purposes, in three animals from each of the NN, TT and W
groups, and in three normal animals 8 weeks after metamorphosis, [3H]proline
was injected into the right eye and the retinotectal projection from that eye
was established autoradiographically.
RESULTS
The assessment of the extent of the bilateral optic fibre regeneration was
based on autoradiographic results from 41 animals, each with one NN, TT or
VV eye (Table 1). Thirteen of the animals were also mapped electrophysiologically. Several animals had to be discarded due to deficient optic nerve
formation from the compound eye, insufficient optic nerve regeneration or
unsuccessful isotope administration. These animals do not appear in the
summary table.
130
R. M. GAZE AND C. STRAZNICKY
Table 1.
Nature
of eye
NN 1
NN 2
NN 3
NN 4
NN 5
NN 6
NN 7
NN 8
NN 9
N N 10
N N 11
N N 12
N N 13
TT 1
TT 2
TT 3
TT 4
TT
5
TT 6
TT 7
TT 8
TT 9
TT 10
TT 11
TT 12
TT 13
TT 14
TT 15
VV
VV
VV
VV
VV
VV
VV
VV
1
2
3
4
5
6
7
8
Regeneration
time
Visuotectal
mapping
Nature of retinal projection
to ipsilateral tectum
Time of RONC:
2 WAM
40 days
40 days
40 days
40 days
40 days
? 30 days
? 30 days
35 days
35 days
3^ months
2^ months
2\ months
2\ months
40 days
40 days
40 days
40 days
40 days
35 days
35 days
42 days
3 months
3 months
3 months
Restricted to caudomedial part
Restricted to caudomedial part
Restricted to caudomedial part (Fig. 3)
Restricted to caudomedial part (Fig. 4)
Restricted to caudomedial part
+
No regeneration to ipsilateral tectum
+
Restricted to caudomedial part
+
Restricted to caudomedial part
+
Restricted to caudomedial part (Fig. 2)
+
Restricted to caudomedial part (? extent)
+
Restricted to caudomedial part
Restricted to caudomedial part
Restricted to caudomedial part
Restricted to rostrolateral part
Restricted to rostrolateral part
Restricted to restrolateral part
Restricted to rostrolateral part
Poor regeneration
+
Restricted to rostrolateral part
+
Restricted to rostrolateral part (Fig. 1)
+
Restricted to rostrolateral part
Restricted to rostrolateral part
Restricted to rostrolateral part
Restricted to rostrolateral part. Normal eye
enucleated 3 weeks before autoradiography
3 months
Restricted to rostrolateral part. Normal eye
enucleated 3 weeks before autoradiography
3 months
Restricted to rostrolateral part Normal eye
enucleated 3 weeks before autoradiography
3-|- months 1\ MAONC Restricted to rostrolateral part.
3^ months 3^ MAONC Restricted to rostrolateral part
Time of RONC:
3 MAM
33 days
33 days
33 days
33 days
33 days
33 days
5 months 5 MAONC
5 months 5 MAONC
Restricted to medial part
Restricted to medial part
Restricted to medial part
Mainly rostromedial (Fig. 6)
Restricted to medial part (Fig. 3)
Restricted to medial part
Restricted to medial part
Restricted to medial part
RONC, right optic nerve cut: WAM, weeks after metamorphosis.
MAM, months after metamorphosis: MAONC, months after optic nerve cut.
Nerve regeneration from compound eyes in Xenopus
131
Table 1 - continued
Nature
of eye
Regeneration
time
TimeofRONC
4 MAM
5 months
9
vv
vv
10
5 months
vv
11
5 months
vv
12
5 months
vv
13
5 months
Visuotectal
mapping
Nature of retinal projection
to ipsilateral tectum
Restricted to medial part. Normal eye
enucleated. 10W before autoradiography
Restricted, to medial part. Normal eye
enucleated 10W before autoradiography
Restricted, to medial part. Normal eye
enucleated 10W before autoradiography
Restricted to medial part. Normal eye
enucleated 10W before autoradiography
Label distribution similar in both tecta - good
coverage.
(a) Short-term regeneration
In nine NN, eight TT and eight VV animals the right optic nerve was
sectioned 2 weeks, 3 months or 4 months after metamorphosis (Table 1). The
visuotectal projection from the operated eye was recorded just after metamorphosis in three TT and in four NN animals to confirm the success of the
initial operation to form the compound eye. All seven recorded animals gave
visuotectal maps characteristic of such eyes. A map from a TT eye is shown
in Fig. 1. The projection is reduplicated about the vertical meridian of the
field and both nasal and temporal extremities of the field project to rostral
tectum while central field is represented on caudal tectum. In projections from
NN eyes the central field was represented on rostral tectum and the nasal
and temporal extremities of the field on caudal tectum (Fig. 2).
The terminal distribution of the regenerating optic fibres on the contralateral
and ipsilateral tectum was assessed by proline autoradiography. Previous
observations have shown that in post-metamorphic animals after section of the
optic nerve, retinal fibres regenerate to both the contralateral and ipsilateral
tecta in about 3-4 weeks' time, and that they fill the whole rostro-caudal and
medio-lateral extent of the tectum (Glastonbury & Straznicky, 1978). The
contralateral projection from a compound eye covers the entire tectum by
about 6 months after metamorphosis. Prior to this time various deficits in the
projection are to be found, depending upon the type of compound eye studied.
These deficits relate to the mode of development of the compound-eye projection
and will be discussed in the next paper of this series (Straznicky et ah, in
preparation). In the present experiments these developmental deficits in the
projections from compound eyes are most obvious in animals with TT eyes,
where there was a small caudo-medial part of the contralateral tectum which
remained uninnervated by fibres regenerating from the compound eye.
132
R. M. GAZE AND C. S T R A Z N I C K Y
Fig. 1. Contralateral visuotectal projection from a TT eye, recorded 2 weeks after
metamorphis. At the end of recording the optic nerve from the TT eye was cut and
allowed to regenerate for 35 days. Autoradiography following administration of
[3H]proline then showed that the ipsilateral tectum was labelled rostro-laterally.
The upper diagram shows the upper dorsal surface of the left optic tectum with
numbers and dots indicating recording positions. The heavy arrow points rostrally
along the midline. The lower diagram shows the right visual field with numbered
rows of stimulus positions corresponding to the rows of tectal positions. The chart
covers 100° of field from the centre to periphery. D, dorsal; N, nasal; Y, ventral;
T, temporal.
Nerve regeneration from compound eyes in Xenopus
133
Fig. 2. Contralateral visuotectal projection from an NN eye, recorded 2 weeks after
metamorphosis. At the end of recording the optic nerve from the NN eye was cut and
allowed to regenerate for 35 days. Autoradiography following administration of
[3H]proline then showed that the ipsilateral tectum was labelled caudally. Mapping
conventions are as in Fig. 1.
j With this exception, fibres regenerating from compound eyes gave a complete
coverage of the contralateral tectum. The similarity of the contralateral projection from compound eyes in animals with and without nerve section and
regeneration indicates that good restoration of the regenerating projection had
occurred by the time of sampling, 30-40 days after optic nerve section.
134
R. M. GAZE AND C. STRAZNICKY
R
L
Fig. 3. Diagrams summarizing the contralateral and ipsilateral retinotectal projections from NN, TT and VV compound eyes, reconstructed from serial transverse
sections of representative brains. In each diagram the arrow points rostrally along
the midline. Top: NN projection, nerve cut 2 weeks after metamorphosis, 40 days
regeneration. The ipsilateral (right) tectum shows no label rostrally. Middle:
TT projection, nerve cut 2 weeks after metamorphosis, 40 days regeneration. The
contralateral (left) tectum shows a small projection deficit caudo-medially,
associated with the age of the animal. The ipsilateral (right) tectum shows label only
rostro-laterally; Bottom: VV projection, nerve cut 3 months after metamorphosis,
33 days regeneration. The ipsilateral (right) tectum shows label only medially. Inset
shows the experimental situation; the left optic nerve, from the normal eye, is not
shown. The right optic nerve, from the compound eye, was cut after metamorphosis
and allowed to regenerate to both tecta. Each projection diagram was constructed
from camera-lucida drawings of every fifth section. The length of the tectal surface
and the extent of label were estimated with a map-measurer and marked on graph
paper. The medio-lateral extent is thus a measured dimension. The rostro-caudal
dimension of the reconstruction was chosen arbitrarily. The edges of sections and
of labelled regions were then joined up and the resulting diagram represents
a flattened view of the tecta and labelled areas.
Nerve regeneration from compound eyes in Xenopus
135
In contrast to the full retinotectal projection on the contralateral tectum, the
i psi lateral tectum became only partially innervated over the same period of
time and the region of tectum innervated reflected the nature of the compound
eye (Fig. 3). Thus NN eyes innervated caudo-medial tectum only (Fig. 4), TT
eyes innervated rostrolateral tectum only (Fig. 5) and VV eyes innervated
medial tectum only (Fig. 6). It is worth noting that the medial and lateral
branches of the optic tract to the ipsilateral tectum are filled to an unequal
extent in these preparations. Fibres from a VV retina enter via the medial
branch of the tract (Fig. 6). Fibres from an NN retina are also most prominent
in the medial tract (Fig. 4) while TT fibres enter the tectum from the rostral
and lateral aspects mainly (Fig. 5).
(b) Long-term regeneration
With long-term regeneration of the optic fibres (2|-5 months) there appeared
to be some slight increase in the extent of the projection on the contralateral
tecta. We were unable to find any consistent spreading of the compound-eye
projections to the ipsilateral tecta. In two NN, two TT and two VV animals
the projections from the operated eye were recorded and the eye was shown
to be compound. In three TT and in four VV animals the left (normal) eye
was enucleated, 3 weeks and 10 weeks respectively, before the animals were
killed. In none of these animals could we detect significant spreading of the
compound-eye projections over the ipsilateral tectum.
DiscussroN
The present experiments were designed to provide information about the
nature of the retina in a compound eye; in particular to ask the question
whether or not each half of a compound eye is a regulated structure in terms
of its map-related cellular specificity. Since we have shown that NN, TT and VV
eyes consistently innervate only the appropriate parts of the ipsilateral tectum
(contralateral to the normal eye), when the compound eyes are induced to
regenerate fibres to this tectum, we can say definitively that these compound
eyes are not regulated structures. Each such eye possesses only the map-related
cellular labels that are appropriate to the type of retinal fragment constituting
the compound eye.
In a normal post-metamorphic animal each eye projects across the entire
contralateral tectum; nasal fibres project to caudal tectum, temporal fibres
project rostrally, ventral fibres project medially and dorsal fibres project laterally
on the tectum. In a post-metamorphic animal with one compound eye, that eye
also spreads its projection across the whole contralateral tectum This is an
abnormal distribution of the optic fibres since they are not confining themselves
to that part of the tectum to which the component retinal fragments would
normally project.
136
R. M. GAZE AND C. STRAZNICKY
V
v .-.«
\
Fig. 4. Dark-field autoradiographs showing the extent of the projection from an
NN eye to both tecta after 40 days regeneration of the optic nerve. Top, rostral;
middle, mid-tectal; bottom, caudal. In each photograph the contralateral tectum is
on the right and the ipsilateral tectum on the left. The contralateral tectum is
labelled in its entirety while the ipsilateral tectum is empty rostrally and labelled
caudo-medially. Calibration, 500 fim for all photographs.
Nerve regeneration from compound eyes in Xenopus
„„
^
»- «B
V
dT
"w^.
Fig. 5. Dark-field autoradiographs showing the extent of the projection from a TT
eye to both tecta after 40 days regeneration of the optic nerve. Top, rostral; middle,
mid-tectal, bottom caudal. In each photograph contralateral tectum is on the right
and ipsilateral tectum is on the left. The contralateral tectum is well labelled except
for a small caudo-medial region. The ipsilateral tectum shows label largely confined
to rostrolateral regions. Calibration for all photographs is 500 fim.
137
138
R. M. GAZE AND C. S T R A Z N I C K Y
Fig. 6. Dark-field autoradiographs showing the extent of the projection from a VV
eye to both tecta after 33 days regeneration of the optic nerve. Top, rostral; middle,
mid-tectal; bottom, caudal. In each photograph contralateral tectum is on the right
and ipsilateral tectum is on the left. The contralateral tectum is well labelled while
the ipsilateral tectum is labelled medially. Calibration, 500 /im for all photographs.
Nerve regeneration from compound eyes in Xenopus
139
The regeneration of optic nerve fibres to restore a well-ordered retinotectal
map involves a selective recognition system between cell markers in the retina
and tectum (Sperry, 1943, 1944, 1945, 1951, 1963, 1965; Attardi & Sperry,
1963; Jacobson & Levine, 1975; Hope, Hammond & Gaze, 1976). We have
shown that the compound eye possesses only a half-set of cell markers
characteristic of the components of the compound eye (nasal, temporal or
ventral). And since we have also shown that fibres regenerating from a compound eye re-establish at once the expanded distribution on the contralateral
tectum which is characteristic of compound eyes, we can say that the distribution
of positional markers on a tectum which has been innervated from the beginning
by a compound eye is different from the normal distribution. The distribution
of markers has become expanded or spread across the tectum and this is a result
of the abnormal innervation; the alteration in the tectal marker distribution
has been brought about by the optic fibres themselves.
In recent papers (Straznicky & Gaze, 1980; Gaze & Straznicky, 1980) we have
demonstrated that fused retinal fragments, such as those forming a compound
eye, retain their original developmental programme related to map orientation.
The present observations provide the strongest evidence yet for the stability
of early retinal programming in Xenopus. Each half of a compound eye is
shown to retain its 'half-ness' in terms of the connections it can later make with
the normal tectum. Thus the map-related cell markers in the retina seem
remarkably stable whereas the tectal positional markers are highly modifiable.
In the next paper of this series (Straznicky et a!., in preparation) we discuss
the development of compound-eye projections and consider the origin of tectal
positional markers.
We are grateful to Mrs June Colville for expert histological assistance.
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SCHMIDT,
{Received 15 April 1980, revised 30 May 1980)