7. Embryol. exp. Morph. 74, 29-45 (1983)
29
Printed in Great Britain © The Company of Biologists Limited 1983
The visuotectal projections made by Xenopus cpie
slice' compound eyes
By D. J. WILLSHAW 1 J. W. FAWCETT 1 AND R. M. GAZE 1
From the National Institute for Medical Research, London
SUMMARY
In Xenopus embryos at stages 28-32 one quarter to one third of the left eye rudiment was
replaced by a similarly sized piece from a different position in a right eye rudiment. Three
groups of operations were performed: (1) temporal tissue was placed in a nasal position; (2)
nasal tissue was placed temporally; (3) ventral tissue was placed dorsally. The visuotectal
projections made by these 'pie-slice' compound eyes were assessed electrophysiologically at
1 week to 6 months after metamorphosis. Of 97 animals, 71 yielded interpretable projections.
In most cases two projections could be identified in each map. One, ascribed to the host part
of the retina, extended over the entire tectal surface mapped. The other, identified as that
from tissue derived from the pie-slice graft, projected to the tectum in register with that part
of the host retina which matched the pie-slice in origin. Both projections were well ordered,
and in the orientation expected if the corresponding piece of retinal tissue had participated in
a normal projection. Consistent differences in pie-slice size and tectal coverage between the
three groups were found. Pie-slices of nasal origin gave maps showing that they came from a
relatively large portion of the retina and projected to a relatively large amount of the tectum;
those of temporal origin occupied relatively small amounts of field and tectum. It was concluded that these results are further evidence for the existence of positional markers in the
retina which are used for the assembly of the retinotectal map.
INTRODUCTION
Analysis of how Xenopus 'compound eyes' project onto the optic tectum has
yielded valuable information about the mechanisms controlling the establishment of nerve connections between eye and brain (Gaze, 1978). Compound eyes
are made by combining two pieces of eye rudiment in the same orbit, to make
an eye of normal size and shape but of abnormal composition (Gaze, Jacobson
& Szekely, 1963). The type of compound eye made is defined by the relative sizes
of the two pieces, their positions of origin and their final positions in the orbit.
Over the past 20 years, there have been many reports about the properties of
compound eyes made from two half retinal fragments (Gaze, Jacobson & Szekely , 1965; Straznicky, Gaze & Keating, 1974). The visuotectal proj ections of these
eyes, when mapped electrophysiologically in the adult, were found to show
systematic abnormalities of ordering. In a compound eye made up of two halves
^Authors' address: National Institute for Medical Research, The Ridgeway, Mill Hill,
London NW7 1AA, U.K.
EMB74
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D. J. WILLSHAW, J. W. FAWCETT AND R. M. GAZE
of matching embryonic origin (such as a double-nasal eye), each half projected
in proper order over the entire tectum, so as to give a double projection (Straznicky & Gaze, 1980); a compound eye composed of two completely dissimilar
halves (such as one constructed from a nasal half and a temporal half) made a
single projection - each half projected to a different region of tectum (Gaze &
Straznicky, 1980). In all these cases each half-eye projected in the orientation
characteristic of its original retinal position; that is, regardless of the final
position of the half-eye in the orbit, the original temporonasal axis of the half-eye
Fig. 1. The normal visuotectal projection from an adult Xenopus. The upper
diagram represents the dorsal surface of the right tectum, with the arrow pointing
rostrally along the midline. Each tectal recording position is indicated by a different
number. The lower diagram represents the visual field of the left eye, which should
be considered as looking out from behind the plane of the paper. The chart covers
100° outwards from the centre. Each number in the field chart gives the optimal
stimulus position for the corresponding tectal recording position. N, S, T, I: nasal,
superior, temporal, inferior. The map is ordered, and in an orientation such that
nasal field projects rostrally and superior field projects medially. Field positions
corresponding to lateromedial rows of tectal recording positions have been-joined by
continuous lines to facilitate map reading. •
Visuotectal projections from 'pie-slice' compound eyes
31
projected rostrocaudally and the original ventrodorsal axis projected
mediolaterally. This is the orientation in which a normal eye projects to the optic
tectum (Gaze, 1958) (Fig. 1).
Studies on these types of compound eye suggest that many features of the maps
from compound eyes are determined by the original, embryonic, positions of the
two eye fragments. It would seem that during normal development each part of
the eye rudiment acquires a. positional value, a unique identity which reflects its
position in the orbit (and remains with it if it is transplanted to form, say, a
compound eye). This set of positional values has the following effects: the
orientation of the partial map made by each part of the retina is specified by its
positional values, and so is independent of the orientation in which the remainder of the eye projects; fibres from cells of similar embryonic retinal origin (i.e.
with similar positional values) are made to share the same piece of tectum
whereas fibres of dissimilar origin project onto different tectal regions.
These conclusions raise a number of questions:
(1) To what extent is the eventual organisation of the map determined by these
positional values?
(2) Are the positional values distributed uniformly around the circumference of
the eye or are they restricted to specific regions?
(3) Can the positional value of a retinal fragment be changed?
(4) How accurately are fibres of similar retinal origin distinguished from those
of dissimilar origin?
Two attributes of a retinal graft have special relevance for these questions: its
position of origin and its handedness. In particular, a 'pie-slice' of tissue transplanted from the right to the left eye will be of opposite handedness to the tissue
of the host eye. In this paper we discuss the electrophysiological maps from pieslice compound eyes involving a change in handedness. Graft experiments in
which the operation does not involve a change in handedness will be discussed
elsewhere (Cooke & Gaze, in preparation).
METHODS
Standard methods of breeding, operating and electrophysiological mapping
were used, as described in detail elsewhere (Straznicky & Gaze, 1980). The
distinctive points of our schedule are as follows.
All operations involved the transplantation of one quarter to one third of a
right eye rudiment into the left orbit of the host from which an equivalent amount
of tissue had been removed (Fig. 2). The operations were carried out between
stages 28 and 32 (Nieuwkoop & Faber, 1956), on embryos anaesthetised in
1:10000 MS 222 (Sandoz, tricaine methane sulphonate) in full-strength NiuTwitty solution. In most cases both host and donor were genetically of wild-type.
In a few cases we used albino tissue as a marker by placing wild-type tissue in an
albino host. The success of the operation was checked 24 h later. The animals
32
D. J. WILLSHAW, J. W. FAWCETT AND R. M. GAZE
were reared at 22-24 °C. They were fed on Boots' liver and vegetable baby food
until metamorphosis and on Tubifex worms thereafter.
The retinotectal projections of the animals were assessed electrophysiologically at ages ranging from 1 week to 6 months after metamorphosis. Recording
was by means of Woods' metal electrodes of approximately 100 K Q impedance
at 1000 Hz. In some cases, transverse sections of the eye and brain, stained by
the Holmes' silver method, were then prepared.
RESULTS
Three groups of operations were carried out. In all operations tissue was
transferred from the right to the left eye. In group 1, a sector from the temporal
pole of a right eye was placed at the nasal pole of the left eye; in group 2, a sector
of nasal origin was placed temporally; in group 3, a sector of ventral origin was
placed dorsally. Grafts into the ventral portion of the eye were not attempted as
this would lead to destruction of the ventral fissure and failure of the optic nerve
to connect with the tectum. Treating right and left eyes as equivalent, in all three
groups the retinal origin of the transplanted sector duplicated part of the host eye
(Fig- 2).
Ninety-seven animals were set up for recording. In 14 of these, responses were
obtainable from seven or fewer tectal positions. These maps had insufficient
Fig. 2. The nature of the operations to form eyes carrying 'pie-slice' grafts.
1. In type 1 grafts, temporal tissue was placed nasally.
2. In type 2 grafts, nasal tissue was placed temporally.
3. In type 3 grafts, ventral tissue was placed dorsally.
Visuotectal projections from 'pie-slice' compound eyes
33
detail to warrant fuller analysis, and are not considered further. In another three
recordings, from albinos, there was an incomplete but otherwise normal map and
no responses could be obtained from the pigmented part of the eye; in a further
nine cases there was a normal or incomplete normal map and there was no
anatomical evidence for the presence of a graft. In these twelve maps there was no
positive evidence that the operation to make a pie-slice eye which had connected
with the tectum was successful. These maps are not examined in detail, but they
will be considered in general terms in the Discussion.
The remaining 71 maps (13 of which involved transplants from wild type to
albino) will now be considered group by group.
Group 1. Temporal to nasal grafts (30 maps - 3 from albinos)
In 27 of the 30 cases of this type, the map consisted of two interpretable
projections. One part-map was in nearly all cases restricted to the rostrolateral
quarter or fifth of the tectum, and was the projection from temporal or temporal
superior field, occupying 75° of the field circumference, which corresponds to
nasal or nasoventral retina (Figs 3-6). In 3 of the 27 cases the extent of coverage
of this projection and the area of retina involved exceeded these figures. This
projection was taken to be that from the pie-slice. In 21 out of the 27 cases there
were enough points in the pie-slice map to determine its orientation, which was
the orientation characteristic of the original retinal position of the tissue from
which it came. The other projection included all the points on the tectum from
which responses could be obtained. In 18 of the 27 cases this was the rostral twothirds of the tectum; otherwise it was the entire dorsal surface. This projection
was identified as that from the host part of the retina. The orientation of the host
map was in all cases normal, but in 10 out of the 27 cases this map was distorted.
The distortions were mostly confined to the boundary between the host and pieslice parts of the map (Figs 5,6).
Of these 27 maps, two were from albinos, and here the area of pie-slice field
as defined electrophysiologically correlated approximately with the area of pigmented tissue in the eye.
There are three other maps in this group. In the remaining albino case the map
was normal but distorted, some responses being obtained from the pigmented
part of the eye; in one case duplications in the map were found, but these were
uninterpretable; in one case two duplications were found embedded in a normal
map.
Group 2. Nasal to temporal transplants (21 maps - 8 from albinos)
In all cases two distinct projections could be identified in each map (Figs
7-10).
The projection from the pie-slice covered much more of the tectum than in the
maps of Group 1. In 14 cases it covered almost the entire tectum (Figs 7, 9);
34
D. J. WILLSHAW, J. W. FAWCETT AND R. M. GAZE
10
Fig. 3.
11
12
13
Fig. 4
Figs 3-6. Four examples of the visuotectal maps from 'pie-slice' eyes of type 1 (in
which temporal tissue had been placed nasally). In all cases wild-type tissue had been
placed in wild-type hosts. Conventions as in Fig. 1, with the additions that the area
of tectum receiving a significant double projection and the area of field adjudged to
be the pie-slice part of the field are each marked off by a heavy line. Filled circles in
the tectum indicate positions from which no response could be obtained. The
reduplicated projection is shown by ringed numbers on the tectum and on the field
chart. In Figs 5 and 6 there is distortion of the host map at the graft/host boundary
and in places the projection seems to have 'compressed' so that a small area of tectum
receives input from a large area of field, e.g. field positions 12, 13, 13, 14 in Fig. 5
and field positions 12, 13 in Fig. 6. The pie-slice occupies the temporal or temporosuperior part of the visual field, corresponding to nasal or nasoventral retina.
Visuotectal projections from 'pie-slice' compound eyes
Fig. 5.
35
Fig. 6.
otherwise it was restricted to the caudal orcaudomedial half or two-thirds (Figs
8,10). The area of retina occupied by tissue derived from the pie-slice, as determined from the map, was also much larger than in group 1. In 12 cases it occupied
the temporal half of the retina (nasal field; Fig. 9), in the other 9 cases a
somewhat smaller portion of the temporal retina (e.g. Figs 8, 10). In 18 of the
21 cases the orientation of the pie-slice map was characteristic of the original
retinal position of the graft. No orientation could be assigned to the other three
maps, because either the map was too disordered or there was insufficient
detail.
The host map had in all cases normal orientation. In all but three cases it was
spread over the entire tectal surface from which recordings were obtained.
36
D. J. WILLSHAW, J. W. FAWCETT AND R. M. GAZE
In two cases there were distortions in the map in the boundary region between
host and graft.
In five of the albino cases there was a good correlation between the extent of
the pie-slice as determined from the map and that given by the pigmentation. In
Fig. 7.
Fig. 8.
Figs 7-10. Four examples of visuotectal maps from pie-slice eyes of type 2 (in which
nasal retina had been placed temporally). Figs 7 and 10 were obtained from albino
eyes containing wild-type pie-slices, Figs 8 and 9 from wild-type eyes. Conventions
as in Figs 3-6. In Figs 7 and 10 the dotted lines drawn between adjacent field
positions indicate that the corresponding tectal positions were not themselves immediately adjacent. Both the area of pie-slice field, situated nasally or inferiornasally, corresponding to temporal or temporodorsal retina, and the area of tectum
receiving a double projection are greater than the areas seen in the projections of
group 1.
Visuotectal projections from 'pie-slice' compound eyes
37
two cases there was a poor correlation, and in one case there was insufficient
evidence to decide.
Fig. 9
Fig. 10
Group 3. Ventral to dorsal transplants (20 maps - 2 from albinos)
In 18 of the 20 cases there was evidence of two distinct projections (Figs
11-14), where the pie-slice projected to rostromedial, caudomedial or medial
tectum. In the 12 cases where map orientation could be determined, the pie-slice
was found to project in the orientation characteristic of the original retinal
position of the graft.
The host projection had in all cases normal orientation. It was free of severe
distortion in all but one case and it extended either over the entire tectal surface
or all but the caudomedial extremity.
In 15 of the 18 cases there was anatomical evidence of a pie-slice. Of these 14
involved wild-type eyes, where the presence of a pie-slice of ventral origin in the
38
D. J. WILLSHAW, J. W. FAWCETT AND R. M. GAZE
N-
Fig. 11.
Fig. 12.
Figs 11-14. Four examples of the visuotectal maps from pie-slice eyes of type 3 (in
which ventral retina had been placed dorsally). Fig. 11 was obtained from an albino
eye containing a wild-type pie-slice; the other 3 maps are from wild-type eyes. In Fig.
13 a large part of thefieldprojects to a small part of the tectum (field positions 1,2,
8, 9). The pie-slice part of the field is found ventrally (corresponding to dorsal
retina). It occupies generally more of the visual field and projects to more of the
tectum than the temporal to nasal grafts (group 1) but less than the nasal to temporal
ones (group 2).
dorsal part of the eye could be recognised by the fact that this part of the eye was
coloured silver and contained the vestiges of a second fissure. In the other case,
an albino eye, wild-type tissue containing a secondary fissure was present in a
dorsal position. There the extent of the pie-slice in the retina, as defined by the
map, correlated with the extent defined anatomically.
In the remaining 2 of the 20 members of this group, there was anatomical
evidence for the presence of a graft. In these animals parts of the graft, as defined
anatomically, projected as parts of a normal map.
Visuotectal projections from 'pie-slice' compound eyes
39
Fig. 14
Fig. 13
DISCUSSION
Our main observation is that the map made by a pie-slice compound eye has
two components, one from the host retina and one from the pie-slice. The host
map was generally well ordered, was normally orientated and extended over the
entire part of the tectum which gave responses.
The pie-slice map was also usually well ordered, and had an orientation
characteristic of the graft's original retinal position. The pie-slice projected to
the tectum in register with the projection from the corresponding part of the host
retina. This observation is in broad agreement with the conclusion drawn by
Conwayefa/. (1980).
40
D. J. WILLSHAW, J. W. FAWCETT AND R. M. GAZE
Distortions and variations between the three groups of maps
Most of the distortions seen in the maps have straightforward explanations. In
a number of cases, a large portion of retina near the graft boundary projected to
a small area of tectum (Figs 5, 6). In other cases, a part of the host map at a
boundary had been tilted with respect to the rest of the host map (Figs 6,12). This
could indicate that there had been compression or rotation of host tissue caused
by the introduction of the transplant. The cases where the graft and host maps
had interwoven are most simply explained as results of interdigitation of grafts
and host tissue. These distortions are also explicable in terms of fibre interactions
driven by the positional disparities created at the boundaries of the pie-slice.
In only 9 of the 27 maps of group 1 (temporal transplants) did the host part
of the retina project across the entire tectum; in maps of group 2 (nasal
transplants) the tectum was entirely covered in 18 out of 21 cases. This difference may be related to the finding that double temporal projections are more
restricted in their tectal coverage than double-nasal projections (Straznicky,
Gaze & Keating, 1981). One possible explanation for this phenomenon is in
terms of the disparate modes of growth of retina and tectum. In a doubletemporal (TT) projection newly arriving retinal fibres have to dislodge fibres
already present at the front of the tectum. This process may slow down the
spread of the projection across the tectum and thus, in young animals, TT
projections should occupy less of the tectum than double-nasal (NN) projections, where newly arriving retinal fibres can simply add on to the newly growing
caudomedial part of the tectum.
In all three groups, the amount of tectum covered by the reduplicated part of
the projection was related to the size of the pie-slice visual field (and hence to
the area of retina derived from the graft): the larger the pie-slice, the larger the
extent of tectal coverage. In the extreme case, when the reduplicated projection
was spread over the entire tectum, the map from the graft-derived tissue covered
half the visual field and thus came from half the retina. This suggests that the
density of terminals on any part of the tectum reflects the density of the parent
cells in the retina.
This variation in the size of graft-derived tissue is not surprising in itself as it
may reflect differences in the size of the pie-slice used from operation to operation. What was striking was the existence of consistent differences in the size of
the graft-derived map (and tectal coverage of these projections) between the
three groups. Pie-slices of group 1 (temporal graft in nasal position) typically
gave rise to maps which represented a 75 ° sector of the eye; pie-slices of group
2 (nasal graft in temporal position) gave maps 120°-180° in size, while pie slices
of group 3 (ventral grafts in dorsal position) gave maps of intermediate size. In
all three cases the intention had been to make pie-slices of one quarter to one
third of the size of the retina. A number of explanations could be offered for this
finding.
Visuotectal projections from 'pie-slice' compound eyes
41
(1) Parts of the eye develop at different rates. This would require that nasal
tissue (group 2) grows more than ventral tissue (group 3) or temporal tissue
(group 1). However, the information available about the growth of the eye
indicates that initially dorsal retina grows most (Gaze, Keating, Ostberg &
Chung, 1979), then ventral retina takes over (Jacobson, 1976; Beach & Jacobson, 1979) and finally temporal retina grows more than nasal retina (Tay,
Hiscock & Straznicky, 1982). More information is required on this point, in
particular concerning the growth of retinal fragments when transplanted to
foreign positions in the orbit. According to Conway et al. (1980), a pie-slice
transplant of ventral origin grows much more than a dorsal transplant of the same
size.
(2) The sequence of positional values originally assigned to the graft becomes
extended beyond the host/graft border. This could involve a reprogramming of
the host tissue at the border. Alternatively there might be cell death at the border
followed by regrowth of tissue, which acquires its positional values by intercalation between the adjoining host and graft tissue (Cooke and Gaze, in
preparation).
(3) The way in which fibres initially form terminations on the tectum is reflected in the way they grow onto the tectum. It is known that the fibres from a TT
eye travel in a tight cluster in the optic pathway, and remain tightly clustered as
they project onto the tectum; the fibres from an NN eye are more widely
distributed (Steedman, 1981; Fawcett & Gaze, 1982). If then fibres interacted
according to current retinal position, the fibres from a pie-slice of nasal origin,
which initially would form a widespread projection, would have a relatively high
chance of projecting next to their current neighbours in the retina. In this way
part of the host would have been effectively recruited by the pie-slice.
(4) There are differences in the ease of doing the operation, which could result
in the grafts being of different sizes, because of different amounts of degeneration or death.
Our data are not adequate to choose between these possibilities, as we lack a
good method of marking the pie-slice part of the eye. We used grafts of wild-type
tissue into albino hosts for this purpose. In just 7 out of 11 albinos in which
responses were obtained from the pigmented part of the eye the size of the pieslice as determined from the anatomy agreed with that calculated from the map.
The problem with this method is that it has not yet been demonstrated that the
presence of pigmented epithelium is a reliable indication that there is wild-type
neural retina underneath. Holt (1980) has suggested that the two structures may
shift relative to one another.
In our maps of ventral to dorsal transplants (group 3), the silver colour of the
dorsal surface of the eye and the presence of a secondary fissure could be used
to indicate the presence of a pie-slice, and these indications correlated with the
existence of a region of double projection in the map. These markers cannot,
however, be used to measure the extent of the pie-slice. Some type of cell marker
42
D. J. WILLSHAW, J. W. FAWCETT AND R. M. GAZE
is required. Possibilities are the tritiated thymidine label used by Holt (1980) to
mark parts of the embryonic Xenopus eye or the use of genetically labelled
polyploidal tissue (Reinschmidt, Simon, Volpe & Tompkins, 1979).
Evidence for the reorganisation of retinal positional values
In 15 cases either a normal or an incomplete but otherwise normal map was
obtained. In 6 of the 15 cases, there was anatomical evidence for the presence
of a pie-slice. In three of these no responses were obtained from the pie-slice,
which suggests that the pie-slice had not connected to the tectum. In the other
three there were responses from the pie-slice, and these formed part of a normal
map. This suggests that the positional values of the pie-slice had been overwritten by those of the host. In the other nine cases (which are not discussed here in
detail) there was no anatomical evidence for the presence of a graft. In these
cases either a reorganisation of retinal values had taken place in the graft or the
graft had failed to connect.
The difficulty in using electrophysiological maps to investigate the role played
by retinal positional values in assembling the retinotectal map is that one piece
of evidence, the nature of the map, is being used to investigate two unknowns:
the state of the retina and the rules for mapping the retina onto the tectum. In
the absence of additional information about one of the unknowns, in the form
of anatomical evidence for the presence and the location of the pie slice in the
eye, the conclusions that we can draw from our results about reorganisation of
positional values are limited.
There is some evidence for large-scale reorganisation in certain types of map
(Hunt & Frank, 1975). These authors found that in compound eyes made up of
two dissimilar halves the transplant projected in an orientation other than that
expected if it had retained its original positional values. This was ascribed to an
effect of transrepolarisation, whereby one half of the retina overprogrammed the
positional values carried by the other. An analogous finding was obtained by
Cooke & Gaze (in preparation) in a recent series of pie-slice maps in which the
graft had the same handedness as the host. Conway et al. (1980) have found a
similar effect. The reorganisation that we have observed is of a different type,
and evidence of this is limited to three cases where the pie-slice projected as part
of a normal projection. There was, however, no evidence of large-scale reorganisation in the pie-slice maps obtained in the early eye rotation experiments
of Gaze, Feldman, Cooke & Chung (1979).
Mechanisms of map formation
Our results agree with the general idea that when a pie-slice is transplanted to
a new position in the orbit it carries with it some record of its original, embryonic,
position.in the orbit. This record is then used in determining the way in which
fibres from the pie-slice are projected onto the tectum; and it must be sufficiently
fine grained to be contained in each quarter of the eye because pie-slices of this
Visuotectal projections from 'pie-slice' compound eyes
43
size were able to make ordered projections. Since we find that the projection
patterns made by pie-slices of different embryonic origin are different, we can
talk in terms of a set of different positional values, encoding position of retinal
origin, assigned to the different parts of the retina. The need for such a differentiation of the various parts of the developing retina according to position
was envisaged by Sperry (1963).
At present it is unclear how retinal positional values are used to assemble the
map. Several authors have suggested that two mechanisms cooperate in map
making: one involving fibre interactions, which arranges fibres in the correct
relative order on the tectum, and one for specifying the orientation of the map
(Willshaw & von der Malsburg, 1979; Law & Constantine-Paton, 1981; Fawcett
& Willshaw, 1982). Both mechanisms are necessary. Our finding that fibres from
a pie-slice eye, which lacks part of the normal retinal complement, project to
parts of the tectum to which they would not normally go requires a fibre interaction mechanism and rules out one involving the matching up of fixed positional
values in the retina with a similar set in the tectum (Sperry, 1963). This conclusion
can also be drawn from previous compound eye results (Straznicky, Gaze &
Keating, 1974) and half-eye results (Straznicky, Gaze & Keating, 1980). On the
other hand, fibre-fibre interaction by itself is inadequate as there is nothing in it
to specify the orientation of the map. Fawcett & Willshaw (1982) have recently
provided direct evidence for the existence of the two separate mechanisms.
The orientation mechanism
As its name implies, this mechanism is one which imparts at least enough order
to the retinotectal projection to specify the orientation of the map. One possibility is that this mechanism operates by arranging the fibres in the optic pathway
in some degree of order so that the fibres are delivered to approximately the
correct region of tectum. This view is supported by the findings that fibres from
different parts of the eye travel in characteristically different parts of the optic
tract and fibres from NN, TT and VV eyes are fed onto the tectum in characteristically different manners (Straznicky, Gaze & Horder, 1979; Steedman, 1981;
Fawcett & Gaze, 1982). We found that the orientation of the pie-slice part-map
was characteristic of the pie-slice's original retinal position. This suggests that the
orientation mechanism responds to the positional value that each part of the eye
carries; see also the discussion on the reorganisation of positional values on
p. 42. The ordering of fibres in the tract could involve fibre-fibre interactions,
but would also require some further information, perhaps from the
diencephalon, to orient the fibre distribution.
The mechanism of fibre-fibre interactions
The most probable site of action for this mechanism in the final ordering of the
map is the tectum itself (Fawcett & Willshaw, 1982). Retinal fibres could interact
with each other by direct contact between their terminal arbors or by means of
44
D. J. WILLSHAW, J. W. FAWCETT AND R. M. GAZE
an electrical or a chemical signal through the medium of the tectum (Willshaw
& von der Malsburg, 1976, 1979; Fraser, 1980). Mechanisms can be conceived
which force each area of tectum to be innervated either by retinal cells which are
themselves neighbours or by retinal cells which have similar positions of embryonic origin; that is, similar positional values.
One set of rules which has been suggested for fibre-fibre interactions is that
the fibres from the two constituent parts of the pie-slice eye behave as separate
populations (Whitelaw & Cowan, 1982). In forming the retinotectal map, the
fibres of each population would interact amongst themselves but independently
of the fibres from the other population. Each population would then map over
the entire tectum, to form a double projection. This idea is contradicted by our
finding that in the cases when the pie-slice constituted less than half the compound eye it projected to a restricted part of the tectum whereas the host part
projected over the entire tectum.
Two general questions remain to be answered about the mechanisms for
orientation and for fibre interactions. The first concerns the relative contribution
that each makes to the precision of the final retinotectal map. It may be that the
orientation mechanism projects the retinal fibres onto the tectum in more than
the minimal degree of order required for orientation. This would be one explanation of our result that the pie-slice map projects in register with that part of the
host map with similar retinal origin. The second question concerns the origin of
the information made use of by these mechanisms. The mechanism of fibre
interaction may use information about original retinal position, which would be
another explanation of the result just mentioned. On the other hand it may use
information about current retinal position. This would provide an explanation of
the stripes made by compound eyes (Fawcett & Willshaw, 1982). There would
then be a conflict between the orientation mechanism which responds to original
retinal position and the fibre-fibre interaction mechanism which responds to
current retinal position.
In conclusion, our experiments on the maps made by pie-slice compound eyes
strongly suggest that each part of the retina acquires, early in development, a set
of positional values which are used in assembling the retinotectal map. We find
that the final size of the pie-slice in the eye and the location and extent of the pieslice projection depends on the position of retinal origin of the pie-slice.
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FRASER,S.
(Accepted 17 November 1982)
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