~~~~e~~ opticus ~ornrn~s~~l~rae po.~teri~r~s pars dor- salis (NOCPd). ..... S. Arnold, F. Roger and G. Sanchez for their techni- cal support, D. Le Cren for his ...
Brain Research Reviews, ll(l986)
221
227-248
Elsevier BRR 90051
The Anatomical Organization of Retinal Projections in the Shark Scyliorhinus Cuniculu with Special Reference to the Evolution of the Selachian Primary Visual System J. REPERANT’.*,
D. MICEL13, J.P. RIO’, J. PEYRICHOUX’,2,
J. PIERRE’ and E. KIRPITCHNIKOVA’
‘Laboratoire de Neuromorphologie, INSERM U 106, Hc?pital Foch, Suresnes and ZInstitutdes Neurosciences du CNRS, Park (France); and 3Groupe de Recherche en Neuropsychologie Exptrimentale, Universitk du Quebec, Trois-RiviPres, Que. (Canada)
(Accepted 18 February 1986) Key words: Selachian - Visual system-Evolution
CONTENTS Introduction
.............................................................................................................................................
228
Materials and Methods .............................................................................................................................. 2.1. Degeneration experiments ..................................................................................................................... 2.2. Radioautography experiments ................................................................................................................ 2.3. Conventional histology .........................................................................................................................
229 229 229 229
Results .................................................................................................................................................... 3.1. Nomenclature .................................................................................................................................... 3.2. Methodology ...................................................................................................................................... 3.2.1. Degeneration methods ................................................................................................................ 3.2.2. Radioautographic methods ........................................................................................................... 3.3. Contralateral visual projections .............................................................................................................. 3.3.1. Optic tract components ................................................................................................................ 3.3.2. Primary optic centers ................................................................................................................... 3.3.2.1. Hypothalamus ............................................................................................................... 3.3.2.2. Thalamus and pretectum ................................................................................................... 3.3.2.3. Optictectum .................................................................................................................. 3.3.2.4. Mesencephalic tegmentum ................................................................................................ 3.4. Ipsilateral visual projections ...................................................................................................................
229 229 229 229 229 231 231 231 231 231 233 238 238
Discussion ................................................................................................................................................ 4.1. Retinal projection in Scyliorhinus ............................................................................................................ 4.2. A common organizational pattern of the primary visual system in selachians ....................................................... 4.2.1. Contralateral visual projections ..................................................................................................... 4.2.1.1. Optic tract components .................................................................................................... 4.2.1.2. Primaryopticcenters ....................................................................................................... 4.2.1.2.1. Hypothalamus ................................................................................................. 4.2.1.2.2. Thalamusandpretectum ..................................................................................... 4.2.1.2.3. Optictectum .................................................................................................... 4.2.1.2.4. Mesencephalic tegmentum .................................................................................. 4.2.2. Ipsilateral visual projections ..........................................................................................................
239 239 239 240 240 241 241 242 243 243 244
Conclusions ..............................................................................................................................................
245
Summary .....................................................................................................................................................
246
Acknowledgements
246
Correspondence:
........................................................................................................................................
J. Reperant, Laboratoire de Psychophysiologie
Sensorielle, I.D.N. Universite Paris VI, 9 Quai St. Bernard, 75005
Paris, France. 0165-0173186/$03.500 1986 Elsevier Science Publishers B.V. (Biomedical Division)
22x .._.
Abbreviations References
.,
.,
,..
_.
_,
1, INTRODUCTION
246
_,
247
(encephalization quotient) was well within the range of that found in birds and mammals4~27~28~‘Y.More-
The more than 800 species which make up the class of Chondrichthyan major vertebrate
..,.,. ._. .._. ..,.
or cartilaginous fish constitute a radiation. These fish, which ap-
peared in the Devonian, into two major divisions:
are traditionally separated the Elasmobranchii or sela-
chians and the Holocephalii4’. On the basis of fossil data and comparative anatomical been proposed 8,9 that elasmobranchs
evidence it has be divided into
4 major groups: Squalomorphii (24% of the total population of sharks), Squatinomorphii (angel sharks), Galeomorphii (73% of all living sharks) and Batoidae (skates and rays, approx. 440 species). All living elasmobranchs probably stem from a common group of neoselachians whose ancestors were ctenacanths’. The relative distribution of primitive and derived traits among modern selachians indicate that the squalomorphs have retained many primitive characteristics whereas the Batoidea have evolved the most from the ancestral condition’. The Holocephalii, which are regarded as the sister group of the elasmobranchs, were abundant during the Carboniferous. Today, they are represented by only 6 living genera. On the basis of their cartilaginous skeleton, chondrichthyans have long been considered to be the ancestor of bony vertebrates, and thus were thought to be the most primitive among modern gnathostoms. Neuroanatomical studies long supported this viewpoint. Numerous classical authors believed that elasmobranchs possessed a simple primitive brain characterized by a telencephalon devoted mainly to olfaction and a midbrain serving as the sole center for visual integration (see refs. 1 and 2 for reviews). At the same time, various behavioral studies32,33.44reinforced this hypothesis and it was concluded that vision in these vertebrates was only a secondary sense. The renewed interest in comparative anatomy during the 1960’s, due mainly to the development of new neurohistophysiological techniques, led to a major revision of these concepts. It was shown that cartilaginous fish possess a large brain and that their brain/body ratio
over,
other
experimental
neuroanatomical
(see ref. 28 for review) provided complexity
of the cyto- and fibroarchitecture
CNS. However,
in-depth
formed on very different a diversity of experimental elucidate
studies
an indication
comparative chondrichthyan techniques
of the of their
studies
per-
species and are needed to
the level of their brain organization
as com-
pared to that of other vertebrate groups. The aim of this study was to define the organization of retinal projections in the shark Scyliorhinus canicula (within this general context). The retinal pathways of selachians have been the subject of several recent experimental investiga~~~~~11.12~18.22.2h~28~30~45.50 . In sharks most of the data have been obtained in galeomorphs, representing the On the other hand, most advanced group L2,1R,22.2h.45. squalomorphs, which retain many of the primitive neoselachian features, have received far less attention*“. The primary optic system of the spotted dogfish, Scyliorhinus canicula, one of the most primitive members of the superorder of galeomorphs, has only recently been examined using selective staining techniques which reveal degenerating axons (Nauta, Fink-Heimer)4”. However, several factors justify a renewed approach to the problem of the organization of projections in this shark species. It is well known that the degeneration technique, especially when applied to fish material, is inconsistent and difficult to Many degenerated optic projecperform 26,30,34,35,38. tions either cannot be stained with the silver methods or the retinal projections cannot be revealed in their entirety. In order to reinvestigate the retinofugal pathways in Scyliorhinw, the present study used a more sensitive neurohistophysiological technique based on the anterograde transport of tritiated tracers. Furthermore, to gain a better understanding of the previous findings obtained with degeneration methods45, these same techniques were again employed in Scyliorhinus. After reviewing the extensive date in the literature and comparing our results, we shall attempt: (1) to
229 define a general pattern ganization examined
of primary
among the different
visual system or-
elasmobranch
and (2) to assess how this pattern
been modified
3. RESULTS
species may have
in the selacian groups at different
3.1. Nomenclature
lev-
els of evolution. Some of the present data have been reported previously in a short communication3’.
published detailed adopted
All experiments
were carried out on fish with snout
water bath temperature
was maintained
by Smeets et al.&. Although cytoarchitectonic
phalo-mesencephalic
2. MATERIALS AND METHODS
to base of tail lengths ranging between
atlas for Scyliorhinus has recently
A brain
40 and 80 cm; at lo-14
“C.
Unilateral retinal ablations were performed under anesthesia (tricaine methane sulfonate) on 6 Scyliorhinus. After survival periods of either 4,6, 1.5,30,40 or 50 days, the fish were anesthetized and perfused with 10% form01 in saline. The brains were removed and stored in the same fixative for l-2 months. The blocks were transferred to a 30% sucrose solution until they sank, then freeze-sectioned at 20 pm in the transverse plane. The sections were processed according to the silver impregnation methods for demonstrating degenerating axons10v16. 2.2. Radioautography experiments Sixteen Scyliorhinus received a unilateral eye injection of 50-100 ,&i in 20 ~1 physiological saline of either lJ3H]proline (spec. act. 27 Ci/mM), rJ3H]leutine (spec. act. 20 Ci/mM), L[3H]fucose (spec. act. lo20 Ci/mM), [3H]adenosine (spec. act. 40 Ci/mM), a mixture of proline and leucine or proline and fucose. The fish were perfused through the heart with 10% form01 in saline. Forty-eight h to 10 days following the injection the brains were embedded in paraffin and cut serially (12 pm) in either the transverse, sagittal or horizontal plane. The sections were coated with Kodak NTB2 emulsion, exposed during 4-6 weeks, developed in D19 and examined under both bright- and dark-field conditions. 2.3. Conventional histology Six normal brains were cut in the transverse or sagittal planes and stained for cyto- and fibroarchitectonic analysis6J5*31,42.
it provides
a
of the dience-
levels of the brain, we have not
the terminology
proposed
to describe
the
different regions to which the retina projects.
For ex-
ample, in both the thalamus
most of
and pretectum
the nuclei defined in the atlas correspond widespread
2.1. Degeneration experiments
description
been
the different
cell masses projection
which rarely sites observed.
to large and coincide
with
In order
to
define the retino-recipient zones in Scyliorhinus, special attention was given to their cytoarchitecture as well as to the topography of the terminal arborizations. Primary visual neuropilar territories containing only a few cells are referred to as optic areas and nuclear structures which receive visual projections are termed optic nuclei. 3.2. Methodology 3.2.1. Degeneration methods No apparent signs of optic
fiber
degeneration
could be observed one week after eye removal. With longer survival periods the silver staining of axon fragments was evident and terminal degeneration appeared as an accumulation of fine argyrophilic granules 30-40 days after retinal ablation. Although the silver impregnation for demonstrating degenerated axons allowed analysis of the general pattern of organization of the optic pathways, it proved insufficient for displaying the overall retinal projections. This was particularly true regarding either the ipsilateral or the contralateral projection to the mesencephalic tegmentum. 3.2.2. Radioautographic methods The radioautographic tracing technique proved to be a much more appropriate tool for revealing retinal projections in this material. Optimal results were obtained with proline, fucose or a mixture of these tritiated tracers. Leucine produced a relatively weaker labeling of the optic tract that was associated with some non-specific terminal labeling. The tritiated adenosine injection resulted in a very weak labeling
230
Figs. 1-4. Darkfield radioautographs of transverse sections through the rostra1 diencephalon 5 davs after injection of 13H]proline into the right eye. Arrows indicate the labeling of optic fibers in the ipsilateral tractus opticus margina& (TOM). Note the bilateral lahcling in the NSC‘. x3X.
231 of the primary
visual system.
days revealed
an incomplete
Survival transport
times of two within the re-
the thalamic emerges
level the tractus opticus basalis (TOB)
from the base of the TOM (Figs. 11, 12).
tinofugal pathways, whereas a 4-day survival period produced the heaviest labeling of the optic centers
This contingent runs rostrocaudally and ventrally, bordering the external wall of the neuraxis and gives
compared
rise to the radix optica ventralis
to the optic tract. Similar silver grain den-
medialis
(ROVM),
sities within both the tracts and centers was obtained 7 days after injection. At the same water tempera-
the radix optica dorsalis medialis
ture,
and RODM are composed of small-caliber fibers and are oriented perpendicularly to the TOB axis (Figs.
equate
the survival labeling
periods
needed
of the retinofugal
to produce pathways
ad-
in Scy-
radix optica basalis (ROB),
liorhinus were longer than those reported for bony fish19*23,34-38, suggesting a lower metabolic rate in this
mus,
the latter
the postero-dorsal
cartilaginous
ROB constitutes
a caudal extension
fish species. Differential
bers of passage and terminal al periods
was the criterion
labeling
of fi-
13, 16, 26). The former innervates
thala-
thalamus.
The
of the TOB. It is
used to distinguish
bers and arborizes within the ventrolateral
portion
of
the posterior
(Figs.
17,
3.3. Contralateral visualprojections
of large-caliber
the ventral
generally
the
composed
and the
fields after short surviv-
tracts from the centers. This is based upon the finding that labeled proteins are first transported to the terminals by the fast axonal flow (see ref. 19 for review). The data derived from the radioautographic method complemented those obtained using the Fink-Heimer technique, making it possible to identify several new visual projection zones. The following description of the primary visual system in Scyliorhinus is based largely on the radioautogram results.
3.3,1.
(RODM)
(Fig. 26). Both ROVM
mesencephalic
myelinated
tegmentum
fi-
21,22). 3.3.2.
Primary optic centers
3.3.2.1. Hypothalamus Nucleus suprachiasmaticus (NSC). The NSC of Smeets et al.46 appears as a single nuclear structure situated within the chiasm between the preoptic area rostrally and the nucleus medius hypothalami caudally. A strong retinal projection attains this nucleus through the TOA fibers (Figs. 3,4).
Optic tract components
At the chiasma the optic nerve appears as 15-20 alternating fascicles of unequal size (Figs. 1, 2). The largest proportion of optic fibers decussate at this level. However, a small ipsilateral fiber contingent is evident (Figs. 1, 2). The contralateral fibers gather along the anterior wall of the rostra1 thalamus and constitute the tractus opticus marginalis (TOM) (Figs. 3, 4, 26). Other axons course medially to the TOM and aggregate into lo-15 small fascicles which are disposed in a fan-like arrangement (Figs. l-3). This visual component, the tractus opticus axialis (TOA), cross-innervates, successively, the anteroventral hypothalamus, the dorsolateral part of the rostra1 thalamus, and the medial pretectum and terminated in the anterior and medial optic tectum (Figs. 14, 1.5). At the pretectal level the TOM subdivides into a tractus opticus marginalis pars lateralis (TOl) and a tractus opticus marginalis pars medialis (Tom). Whereas the TOm projected to the central pretectum and medial optic tectum, the TO1 supplies the lateral and dorsal optic tectum (Figs. 26, 27). At
3.3.2.2. Thalamus andpretectum Nucleus opticus dorsolateralis anterior thalami (NODLAT). This nucleus is located within the rostral thalamus dorsal to the TOM. It is slightly ovoid and composed of a cellular ring, surrounding a neuropilar center rich in optic terminals. It is innervated laterally by the TOM and medially by the TOA (Figs. 5-7). Nucleus opticus dorsomedialis anterior thalami (NODMA T). Situated laterally and in close proximity to the NODLAT, this small nucleus spans the sulcus ventricularis dorsomedialis medially. It is triangular in shape, contains numerous cells, and receives a weak optic fiber input via the TOA. The NODMAT appears to be equivalent to the rostra1 part of the thalamus dorsalis pars medialis of Smeets et al.46 (Figs. 5.26). Nucleus thalamicus tractus optici marginalis (NTTOM). This nucleus has a poorly defined cytoarchitecture and is completely inserted within the TOM. It extends from the midthalamus to the pretec-
232
233
isstrongly innervated by collaterals of the TOM (Figs. 8,9,26). Nucleus opticus ventralis thalami (NOVT). The NOVT extends from a region eaudal to the NODLAT to the posterior thalamus. ~ytoarchjte~toni~ally heterogeneous, this visual center can be subdivided into: a thick pars lateralis region displaying a high cell density and a pars medialis or periventricularis composed of 2 or 3 compact cell laminae. It could correspond in part to the thalamus ventralis pars lateralis and pars medialis of Smeets et a14’j.The anterior part of this visual afferent zone, which is adjacent to the TOM laterally, exhibits a somewhat triangular shape in transverse sections. More caudally, the NOVT lies beneath the TOM and is roughly rectangular. This nucleus is innervated by the ROVM but visual input is weak (Figs. lQ-14,16,20)+ N~&~e~ opticus dorsffl~ posterior thffl~rn~ (NODPT). Less extensive than the NOVT, this structure is innervated by the RODM and contains few optic terminals. The NODPT appears rostrally where the posterior commissure is fully developed. Here, it joins the TOM laterally. Throughout the full posterodorsal expanse of the thalamus, this nucleus exhibits a roughly triangular shape and lies over the sulcus di~n~phali~us dorsalis 2 of Smeets et al.‘@.At its anterior and intermediate levels, the NODPT is composed of two cytoarchitectonically different substructures: (1) a wide pars lateralis with high cell density and (2) a small pars periventri~ularis composed of several compact cellular columns. Mare caudally, where the intertectal commissure disappears, the retinal input to the NODPT is less extensive. The NODPT is the equivalent of the posterodorsal part of the thalamus dor~medialis of Smeets et al.@‘.It is also conceivable that this structure belongs to the pretectum; correspondingly, its substructures (pars lateralis and pars periventricularis) would represent the nucleus l~ntiformis praetectalis pars externa and pars plicata, respectively, as defined by Farmerr (Figs. 14,16,26). Nucleus opticus pretectalis centralis (NOPC). This
tal region and
celt-poor nucleus lies at the base of the anterior optic tectum and is crossed and innervated by the Tom. Although dense in its rostra1 portian, the retinal projection becomes thinner caudally (Figs. 13, 14, 16, 26). Nucleus opticus commissurue posterioris pars dorsalis (NOCPd). Localized in the dorsomedial pretecturn just below the posterior commissure this visual structure is ~ytoar~hite~toni~ally ill defined. The TOA crosses through and innervates the nucleus; in addition, optic fibers belonging to the TOm enter it laterally and arborize (Figs. lo-15,26). Nucleus opticus c~mm~sur~e paster&k
pars ven-
tricular& (~UCPv).
This small, round primary visual zone lies medially beneath the posterior commissure and above the fasciculus retroflexus. Within the nucleus, numerous basophilic neurons are disposed in columns and receive a weak retinal projection. The NOCPv is innervated by a posterior branch of the TOm (Figs. 16,26). X3.2.3. Optic tect~m From the outer surface inwards, the optic tectum of Scyliorhinus is composed of 7 layers or principal strata. (1) The stratum marginale (SM or layer 1) is thin and lacks cell bodies; (2) the stratum fibrosum et griseum superficiale (SFGS or layer 2) is of medium thickness and can be divided in two sublaminae, a relatively cell-free superficial component (SFGSs) and a cell-dense inferior bmina (SFGSi); (3) the stratum griseum superficiale (SGS or layer 3) is thick and packed with cells; (4) the stratum fibrosum et griseum centrale (SFGC or layer 4) is relatively thick and cells are dispersed; (5) the stratum album centrale (SAC or layer 5) contains many fibers; (6) the stratum griseum pexiventriculare (SGP or layer 6) is thin and made up of 3 compact cellular laminae and (7) the stratum fibrosum periventriculare (SFP or layer 7) is a thin lamina close to the ependymal layer and is rich in fibers. Both TOm and TO1 fibers as well as some TOA fibers enter the optic tectum at a right angle to the surface and then arborize within the
Figs. 5,7,8. Brightfield radioautographs of transverse sections through the diencephalon 4 days (Figs. 7,s) and 7 days (Fig. 5) after intraocular injectian of (3H]proline. Fig. 5 can be compared to Fig. 26A. x50 (Fig. 5); x 185 (Figs. 7,8). Fig. 6. Transverse section through the rostra1 thalamus stained according to Bodian, illustrating the cytoarchitecture of the nucleus opticus dorsofateraIis anterior thatami. x 12.5. Fig. 9. Degeneration in the NTTUM contralateraal to the retinal ablation, 30 days postoperative survival, transverse se&cm, Fink-Heimer stain. X3.20.
-.-*.. ” i
b
-n/L
012 Figs. IO- 13. Bright- and darkfield radioautographs rior pretectum (Figs. 12. 13) 6 days after injection tively. to Figs. 2hB and 26C. X3X.
of transverse of [‘Hjproline
6;ections showing labeling in the thalamus (Figs. 10. 11) and the antcinto the right eye. Figs. IO. 11and 17. Ii can he compared. respcc-
Fig. 18. Fig. 19. sence of Fig. 20. solution
Photomicrograph of transverse section through the optic tectum, normal material, Fink-Heimer preparation. x 120. Photomicrograph of transverse section through the mid-medial optic tecta 30 days after right retinal ablation. Note the abdegenerated optic fibers in the ipsilateral tractus opticus marginalis pars medialis (TOMi). ~260. Brightfield radioautograph showing labeling in the contralateral optic tectum 5 days after intraocular injection 01 :I combined of [‘Hlproline and [‘H)fucosc. x 110.
237
Figs. 21-23. Darkfield radioautographs (transverse sections) showing labeling in the midbrain region 5 days after [3H]proline injection into the right eye. Fig. 21 can be compared to Fig. 26G. The arrow (Fig. 23) indicates the labeling of optic fibers in the ipsilateral optic tectum. x38 (Fig. 21); x98 (Fig. 22); x48 (Fig. 23).
Figs. 24,25. Darkfield radioautographs of transverse sections through the rostra1 thalamus (Fig. 24) and pretectum (Fig. 25) 5 days aftcr [3H]proline injection into the right eye. ~48 (Fig. 24): x34 (Fig. 25).
SFGS and superior portion 18-20.23.26). 3.2.2.4.
Mesencephalic
Area
optica
of the SGS (SGSs) (Figs.
tegmentum
tegmenti
mesencephali
dorsalis
caudoventral mesencephalic tegmentum: the NOTMv. Its lateral part (NOTMvl), composed of neuropil, displays numerous optic terminals, whereas its more extensive medial aspect (NOTMvm) contains fewer optic endings (Figs. 21,22,26,27).
(AOTMd).
Caudal to the posterior commissure at the level where the tectal ventricles appear, the basal optic root (ROB) which courses in a ventral direction, is separated from the optic tectum by a wide external structure: the nucleus profundus mesencephaIi. At this level, a thin fascicle emerges from the ROB and extends dorsomedially. This optic contingent arborizes in the AOTMd, an ill-defined area which displays few cell bodies and is located in the rostrodorsal mesencephalic tegmentum between the nucleus profundus mesencephali laterally and the nucleus interstitialis medially (Figs. 17, 26, 27). Nucleus opticus tegmenti mesencephali ventralis (NOTMv). The main trunk of the centrocaudally directed ROB terminates in a large structure in the
3.4. Ipsilateral visual projections A discrete ipsilateral retinal projection was clearly evident in most of the radioautographic preparations. Ipsilateral fibers were observed within the axial and marginal tracts. Labeled ipsilateral optic terminals were present at the hypothalamic (NSC), thalamo-pretectal (NODLAT, NTTOM, NOVT, NOPC, NOCPd) and tectal levels. Within the latter region the label was present in the anterior SFGS. The intermediate optic tectum is completely devoid of optic terminals. In contrast, the caudal part exhibits a small zone of retinal input restricted to the medial SFGS. It is conceivable that this zone corre-
239 sponds to the recrossing to the ipsilateral the ipsilateral tures
listed
of contralateral
side. With the exception
visual projection above
tectal fibers
transport
of the NSC,
ment to another,
to the different
is extremely
weak
(Figs.
struc1-4,
was remarkably especially
case was used; (3) although
from one experi-
when proline
and/or fu-
the background
silver grains were high in some specimens, labeling was detected
23-27).
constant
levels of no specific
in any of the structure
situated
close to the primary visual centers to which the retina 4. DISCUSSION
strongly projects.
4.1. Retinalprojections in Scyliorhinus
grams and in the Fink-Heimer preparations the inferior limit of retinal fiber arborization within the tec-
Correspondingly,
in the radioauto-
turn was always the same (SGSs, Figs. 19,20). Compared
to Smeets’ results45 and to the present
data obtained radioautographic
using the degeneration method supplied
about the organization
technique,
more information
of the primary
in Scyfiorhinus. Only 6 contralateral
the
visual system optic terminal
structures have been identified with degeneration techniques. However, 12 different visual centers could be differentiated in the radioautographic preparations, including new-found visual ipsilateral projections to the thalamic, pretectal and tectal levels. The primary contralateral visual centers already identified in this species with the degeneration method (ref. 45, present results) were the NSC, NODLAT, NTTOM, NOVI, NOCPd and the superficial tectal layers. These last have been described by Smeets45 as the nucleus suprachiasmaticus, thalamus dorsalis pars lateralis, corpus geniculatum laterale, nucleus pretectalis, stratum medullare externum and stratum cellulare externum of the optic tectum. Moreover, these methods revealed only an ipsilateral opto-hypothalamic projection (ref. 45, present resuits). The question remains as to whether the new projection sites demonstrated with the radioautographic method indeed represent retinal projection zones or whether they correspond to transneurally labeled zones that have taken up the tracer from the optic terminals. Several arguments make it possible to reject the latter hypothesis: (1) the labeling of the different contra- and ipsilateral visual centers observed following the intraocular injection of tritiated precursors occurred within 4 days. However, transcellular transport has not been observed to take place in ectotherms before 11 days of surviva123~24~36,even when they are maintained at a temperature approximately twice that used for the sharks in the present experiments; (2) if transport occurs, the labeling should vary, notably as a function of survival time, but tracer
newly identified strated
contralateral
optic centers
with the radioautographic
method
labeled as a result of the transneuronal tiated material
from the optic terminals,
If the demon-
has been
leakage of trithen the la-
beling of deep tectal layers should also have been observed, but this was never the case; (4) this lack of labeling also supports the existence of an ipsilateral retinal projection in Scyliorhinus. Other observations reinforce this possibility: (a) optic fibers could be traced ipsilaterally directly from the labeled optic chiasm and (b) similar results were recently obtained after intraocular injection of either HRP or Fast blue (Rep&ant, unpublished observations). 4.2. A common organizational pattern of the primary visual system in selachians In selachians, the first observations with conventional light microscopic techniques indicated a crossed thalamic and tectal projection from the retina1-3,7.17,20.21.47. However, the organization of the selachian primary visual system has recently been re-examined employing new neurohistophysiological techniques in 7 shark species and 4 species of skates and rays. Six of the sharks examined (Ginglymostoma cirratum ‘2.26 Galeocerdo cuvieri l2, Negaprion brevirostris l8, Mktelus canis28 Scyliorhinus canicuIa37,45.46,Hemiscyllium plagioium22) belong to the group of galeomorphs, whereas only one squalomorph (Squafus acanthias28.29)has been investigated. The 4 Batoidea examined (Rhinobatos product&‘, Platyrhinoidk triseriata3’, Raja clavata45*50and Raja egfanteria”) are rajoid. Though these forms represent only a few species, the new experimental findings from them have led to a considerable revision of classical thinking. The topography of retino-thalamic and retino-tectal projections has been more accurately described and some new primary visual centers
240
NODLAT
TOI
D
241 have been localized
at the hypothalamic,
and tegmento-mesencephalic
levels.
pretectal
Moreover,
the
presence of an ipsilateral visual contingent has been demonstrated in several species. In spite of various difficulties related to the diversity of cytoarchitectonic nomenclatures and to the diversity of cytoarchitectonic nomenclatures techniques
and to the variety of hodological
employed,
a comparison
data clearly points to the presence common pattern
or organization
of the different of a unique
and
of the primary visu-
fascicle of the basal optic tract28,29. Elsewhere, cyllium have noted and illustrated
this tract without
specifically naming it. The ROVM has also been identified in several selachians. In Rhinobatos, Ebbesson and Meyer” referred to it as a fascicle of the ventromedial nucleus; in Squalus, Northcutt29 called it as a dorsal fascicle of the basal optic tract. It has also been designated RODM
al system in selachians.
both
Luiten26 in Ginglymostoma and Jen et al.22 in Hemis-
described and illustrated without being in various other selachians22~26~30. The
has rarely been observed:
in Ginglymosto-
ma, Luiten noted the tract (ref. 26, Fig. 2G) but did 4.2.1,
Contralateral visual projections
4.2.1.1. Optic tractcomponents The TOM (optic tract26, lateral optic main optic tract’) and its two posterior TO1 (dorsal optic tract3’) and TOm tract3’, dorsal fascicle of the medial described have been
not designate 4.2.1.2. tract18*29345 or subdivisions: (ventral optic optic tract29)
previously7~11~‘2~17~18~22~28-
The TOA (medial optic tract22326, ventral fascicle of the medial optic tract29) has also been observed in several sharks and ray species (Ginglymos-
30-37,45-46.
Primary optic centers
4.2.1.2.1. Hypothalamus Nucleus suprachiasmaticus (NSC). A visual projection to the anterior hypothalamus has been reported in all of the species examined, regardless of the tracing methods employed. This region is com-
Scyliorhinus
toma cirratum 26, Hemtkcyllium plagiosum 22, Mustelus canis28, Scyliorhinw canicula 37*4s, Squalus acanthias28,29 Raja clavata45). The ROB has generally not been observed in degeneration studies (Ebbesson and Meyer ” in Rhinabatos productus, Graeber and Ebbesson” in Negaprion brevirostris, Ebbesson and
canicula)
HYPOTHALAMUS --___-_----
Ramsey l2 in Ginglymostoma cirratum, Smeets45 in Scyliorhinus canicula). In contrast, in all selachian species the use of techniques involving axonal transport of different tracers has clearly demonstrated its presence 22.26,28*29,37350, although different terminologies have been used: accessory
it by name.
THALAMUS
optic tract3’, ventral
PRETECTUM
ror TECTUM
Fig 26. Schematic representation illustrating retinal projections in Scyliorhinrrs canicutafrom the rostra1 diencephalon (A) to the caudal mesencephalon (G&taken from transverse sections of Fink-Heimer and radioautographic preparations. The passage of optic fibers is indicated by dashed lines and optic fiber terminals are shown by fine dots.
Fig. 27. Diagram of retinofugal pathways in Scytiorhinwcanida.
242 parable from one species to another, although different nomencIatures have been used: nucleus chiasmaticus’2, nucleus preopticus4s, cleus”,
hypothalamic
optic nu-
preoptic area2*.*‘, and nucleus suprachiasma-
described
a projection
the level of the posterior
and Wathey””
to the caudal hypothalamus
lateralis
diencephalij,
corpo genico-
sponds in part to the lateral geniculate
tiCus”Z.3n.37
In Plutyrhinoid~s, Northcutt
pus geniculatus
lato laterale”?. nucleus opticus lateralis2”. and superficial pretectal nucleus”-?“. The NTTOM also corre-
have at
tuber.
nucleus of Eb-
besson and Ramsey” and of Graeber and EbbessonlX as well as to the dorsolateral optic complex of Ebbesson and Meyer”.
Another
may be the nucleus
equivalent
geniculatus
of the NTTOM
praetectalis
of Farn-
er13. 4.2.1.2.2.
Nt4cleu.s opticus ventralis thalami (NOVT). This re-
Thalamus andpretectum
Nucleus
opticus dorsoLateralis anterior thalami
(NODLAT). contralateral
Numerous studies have described a retinal projection in a region of the ros-
tral thalamus which is in some respect comparable
to
the NODLAT. However, the cytoar~hitecture of this structure has not always been clearly defined and its possible equivalents have been given different names: (1) the anterior part of the thalamus rostralis pars lateralis28~29~4s~~,(2) lateral part of the anterior thalamic nucleus30 and (3) anterior part of the pretectal area*(‘. Conceivably, the NODLAT may correspond in part to the ventrolateral nucleus of the optic tract of Jen et al.“’ and to the nucleus geniculatus lateralis of Farner’4. It should also be noted that the NODLAT has been included as part of: (1) the lateral geniculate nucleus of Ebbesson and Ramsey” and Graeber and Ebbesson’“, (2) and the dorsomedial complex of Ebbesson and Meyer”. Nucleus opticus dorsomedialis anterior thalami (NODMAT). The existence of a contralateral retinal projection to a region identical to the NODMAT has previous been described in 3 studies. Nevertheless, it has not been defined as a distinct entity, but rather has been included as part of different primary optic centers in the vicinity of the NODMAT. For Northto cutt and Wathey”“, the NODMAT corresponds the most medial part of the anterior visual thalamic nucleus, whereas for Jen et al.” and Luiten”’ it corresponds to the rostromedial part of the pretectal nucleus and the pretectal area, respectively. Nucleus thazamicus tracts optici marg~na~is (NTTOM). This primary optic nucleus has been described in many selachian species by all of the classical and modern investigators with the exception of Jen et al.22 and Luitenzh. Different terminologies have been employed: nucleus geniculatus*‘, lateral nucleus geniculatus lateralis geniculate nucleu9, pars dorsalis17, corpus geniculatum laterale’“.““, cor-
gion has been
species adopted:
and
distinguished different
ventrolateral
in numerous
nomenclatures optic nucleus”“‘,
selachian have
been
ventral tha-
lamic nucleus2R*2y, ventrolateral and ventromedial thalamic nuclei. “‘. thalamus ventralis pars lateralis”. With the exception of the data provided by Northcutt and Wathey’“, the NOVT has not been described fully. Graeber and Ebbesson’8 and Ebbesson and Meyer” observed only its anterior part, whereas others, such as Northcutt’“s2” and Smeets”“. identified visual terminals essentially in its lateral portion. Nucleus opticus dorsalis posterior thalami ~NO~PT~. This structure has been observed in only in two species: Squalus acant~ias (Northcutt~~.~‘) and Ginglymostoma cirratum (Luiten”). The latter author described and illustrated (ref. 26, Fig. 2G) this region without specifically naming it. Moreover, in squads the NOPDT was incorporated into the posterior and lateral parts of the central pretectal nucleus (NorthcuttzY, Figs. 3B and 4A), which is the equivalent of the NOCPd. Nu~~e~~sop ticus prete~ta~~s~entralis (NO PC). The NOPC has been described in several selachian species and referred to as the posterior optic nucleus’2,‘8.26 or the central pretectal nucleus3”.J. ~~~~e~~ opticus ~ornrn~s~~l~rae po.~teri~r~spars dorsalis (NOCPd). This nucleus has been identified in most experiments performed in selachians and named variously: pretectal area or nucleus’2.‘X.‘h.‘5, dorsonudeus pretectalis perivenmedial optic nucleus”. tricularis pars dorsalis”“, central pretectal nucleus”” (in Mustelus) and anterior part of the central pretectal nucleus28,2y (in Squatus). Nucleus opticus commissurae posterioris pars ventratis ~NO~Pv~. North~utt and Wathef” have described a contralateral projection on a structure that is equivalent to the NOCPv and have called it ventral periventricular pretectalis nucleus.
243 4.2.1.2.3. Optic tectum A contralateral retinotectal
radiographic projection
in selachi-
methods
(ref. 37, present
only failed to differentiate
results),
not
the SM but also revealed
ans was reported very early by various classical authors1-3~7~17~20~21*25*47. More recent experimental stud-
argentophilic granules which were interpreted either as degenerated optic terminals45 or as artifacts (pres-
ies have confirmed and refined tions11~‘2~18,22,26,2’-30,3’,45,46,50 It is
perficial
that the contralateral
optotectal
these generally
projection
observaagreed
arborizes
within the superficial layers. However, the precise delimitation of this region can differ markedly between authors. techniques,
The use of highly diverse histological
which are often unsuitable
strating such a projection,
and of different
tures (see Table I) to describe
for demonnomencla-
the tectal lamination
ent results) which were localized within the most suzone of the tectum
topographically
corre-
sponding to this stratum. Classical data are particularly contradictory regarding the limit of the inferior boundary to which the retina projects (SAC21, SFGC1,2,7,25,43,SGC”, SFGSs4’), but the same contradictions
also exist in more recent
results
obtained
using the same experimental techniques (SFGC’2,‘8,26,50, SFGSi22.28, SFGSs28,3’,45,46). These
appear to be the main causes of these discrepancies.
discrepancies
The repeated use of conventional fibroarchitectonic or Golgi methods’~7~‘4~‘7~20~21~25~43~47 has failed to dem-
ical differences but rather to interspecific variations in the structural organization of the tectum. The comparative histology of the selachian optic tectum has been shown to display a wide range of architectonic diversity27*30,40,46. This variability would, in
onstrate this projection clearly. For example, according to Sterzi ‘47, the optic fibers arborize only in the SFGSs, whereas for Houser” they spread from the SM to the SAC. Elsewhere, the SM alone or together with the SFGSs, considered as visual zones1,2.7.‘7. 21,25,43have sometimes been described as the layers receiving fibers from the TO1 and TOm’.2,7*21.25.The use of experimental tracing techniques has allowed an extension and a revision of these data. It has thus been demonstrated that the optic fibers do not enter the optic tectum via its external aspect but run within the tectum towards the outer surface and arborize in the superficial layers 11,12,18,22.26-30,37,45,46,50.For SOme of these authors27-30,37*50, the external boundary of the SFGSs constitutes the superficial limit of optic arborization. Indeed, no optic terminals have been found to be present in the SM (refs. 27-30, 37, 50, present results). For others12J6*22’26,45the optic projection attains the most superficial tectal region and consequently the SM. Since they used degeneration methods, these latter authors failed to recognize this layer as a distinct entity. In fact, they always represented the SM as an integral part of the SFGS’2.‘8,22,26.45.It is likely that the SM is both present in all selachians examined and devoid of optic endings. The failure to identify this strata in some species could be due to the fact that it is very thin and hardly distinguishable. Moreover, the degeneration methods seem to be less accurate for defining the superficial limit of the retinotectal projection. For example, in Scyliorhinus canicula, degeneration methods (ref. 45, present results), in contrast to auto-
are not necessarily
due to methodolog-
part, also explain the numerous nomenclatures used to describe the tectal lamination in selachians (see Table I). Generally, a dense population of neuronal bodies has been observed within the deep tectal regions of the most primitive chondrichthyans (Holocephalii and Squalomorph sharks). In contrast, in the higher, more evolved forms (galeomorph sharks, skates and rays) these neurons appear to have migrated to the neuropil of the superficial layers. A disruption of tectal lamination occurs concomitantly with the formation of new cellular layers. Consequently, in archaic forms (e.g. Squafus acanthias29) the optic fibers arborize within regions that are devoid of neurons, whereas in more evolved species (i.e. Mustefus canis28) this projection terminates in the neuron-rich superficial Scyliorhinus canicula.
tectal layers as shown in
4.2.1.2.4. Mesencephalic tegmentum Area optica tegmenti mesencephali dorsalis (A 0 TMd) . Northcutt28~29 in Squalus acanthias and Luiten26 in Ginglymostoma cirratum have described and illustrated this zone of retinal projection without specifically designating it. In some respects the AOTMd seems to be equivalent to the dorsal accessory nucleus of Platyrhinoidis triseriata3’. Nucleus opticus tegmenti mesencephali ventralis (NOTMv). This primary visual center has been identified in numerous selachian species mainly in experi-
244 TABLE I Comparison of selachian tectal nomenclature
Houser 1901
Catois 1902
Kappers et al. 1936 Ebbesson and Ramsey 1968 -_
-Zone des fibres nerveuses myeliniques superficielles
Gerlach 1947
Stratum medullare externum
Superficial zone
Kernarme molekularschicht Layer 6
Zona externa Middle zone Zona interna
Deep zone
OU
centrale Stratum medullare profundum ‘ICentral gray
matter
I
Couche des fibres nerveuses myeliniques i profondes
Strato midollare intern0
Stratum medullare internum
Zone ou couche / granuleuse
Strato cellulare intern0
Stratum cellulare internum
ments which have The two subdivisions
Strato limitante intern0
used axon tracers22~26.2R.29.37~50. noted in the NOTMv of Scylior-
hinus in the present study have never been described. Various nomenclatures have been employed to designate this tegmental nucleus: nucleus of the basal optic root”, basal optic nucleus26~28~29,ventral accesoptic nucleus”, sory optic nucleus3’, ventromedial nuectomamillary nucleus12 and visual tegmental cleus2’. 4.2.2. Ipsilateral visual projections Classical authors reported that the selachian optic chiasma decussates completely’-3~7~‘7*20~21~47. However, most of the experimental data collected in recent years and derived from many different species points to the retinohypothalamic projection11~‘s~28-“o~37~45~46. Two radioautographic studies performed in the batoid Platyrhinoidi.s3’ and in the shark Hemiscyllium22 have demonstrated the presence of a denser ipsilateral projection as is the case for Scyliorhinus. In Platyrhinoidk12, different retino-recipient cell groups re-
m Nz 5 Opticus Fasern Layer 5 :c !Bk ak Iwe,
I c! j;
Hauptzellenschicht Layer 4
/ Leghissa 1962
Zona grigia e fibrosa externa ~Strata S-8
I Zona bianca e grg&
__ .-.. ~~~ -_ i, stratum 4 Lamina medullaris 1 interna Layer 3 ---I Lamina cellularis Zona grigia interna Laver 2 Je fibrosa esterna Lamina periventriStrata 1-3 kullre Layer 1 7
ceiving ipsilateral fibers have been identified at the hypothalamic, thalamo-pretectal, tectal and tegmento-mesencephalic levels. In Hemiscyllium, only 3 such ipsilateral visual projection zones have been reported (NSC, NODLAT, SFGS rostra1 and posteromedial). In Scyliorhinus, an intermediary arrangement is observed since the ipsilateral contingent was shown to innervate 7 structures at the hypothalamic, thalamo-pretectal and tectal levels. Such differences may reflect authentic interspecies variation in the organization of the ipsilateral visual projection in selachians, although this would need to be clarified by further investigations. On the other hand, the difference might be linked to the experimental methods employed. For instance, the degeneration-staining method used in some of the studies may not be as sensitive as the radioautographic method in revealing this projection. This would explain the failure to demonstrate uncrossed projections in those studies using the former methods. However, there is evidence that the radioautogra-
245 TABLE I (continued) Schroeder and Ebbesson 1975 Luiten 1981 Stratum medullare externum Layer A
Stratum cellulare externum zona externa Layer B
Farner 1978
Witkovsky et al. 1980
Smeets, 1981 Smeets et al. 1983
Rep&ant et al. 1984 Present results
‘)
Marginal layer
Stratum medullare externum
Stratum marginale Layer 1
1
Layer 1
Stratum fi- (pars brosum et 1externa, griseum supars perficiale interna Laver 2 1
Layer 13
rI
Zona externa Layer 2
Optic
Layers
fiber
I I
I
12-10
zona
layer
interna Layer 4 s w -!
-L
I
i Stratum album centrale Layer 5
Layer 3
Central zone
Stratum medullare internum Layer 4
Layer 2
Periventriculare zone
Stratum cellulare internum Layer 5
Stratum griseum periventriculare Laver 6
Stratum fibrosum periventriculare Layer 6
Stratum fibrosum
Stratum centrale Layers 8-6
Stratum fibrosum et I griseum centrale 1 Layer 4
Layer 3
Layer 1
phic technique may also be ineffective in revealing a discrete projection. This probably depends on the total amount of tritiated precursor injected into the eye and on the amount taken up and transported by the retinal ganglion cells. For example, in birds the radioautographic method has failed to demonstrate the existence of a small ipsilateral retinal contingent, whereas other techniques (HRP, HRP-WGA, Cobalt and RITC) have done ~0~s~‘. 5. CONCLUSIONS
Comparison between the different sharks, skates and rays thus far examined supports the notion of a consistent and general pattern or organization of the primary visual system in all selachians (at least with regard to the contralateral projections). The most notable differences observed, which were first interpreted as interspecific variations, seem instead to be
related
1
to the technique
ports on the selachian
employed. primary
Since
visual system
earlier
re-
often
de-
only a crossed retinotectal projection, it was thought to represent the most primitive form of primary optic system among gnathostom vertebrates. However, it is now evident that the pattern of organization of the selachian retinal projections displays a high degree of complexity similar to that found in some actinopterygians and amniote vertebrates. Although the topographical localization and number of scribed
optic terminal zones are approximately the same in sharks and batoids, the important differences among them are mainly linked to variation in the architectonic organization of these centers. In squalomorph sharks, the retino-recipient zones have a neuropillike structure and the optic terminals must make contact with the long and winding dendrites of neurons whose cell bodies lie in the vicinity of the ventricles. In most galeomorph sharks and batoids, the postsyn-
346
aptic neurons
to the optic fibers appear
to have mi-
grated towards the periphery, where they constitute visual structures that are either nuclear or stratified.
tectum (SFGS, SGI) and mesencephalic tegmentum (AOTMd, NOTMv). Ipsilateral retinal projections were found to arborize within 7 distinct zones at the
The cumulative
hypothalamic
data suggest that the selachian
mary visual system has not evolved crease in the number through
of projection
an architectonic in the number
structures dritic
of these cen-
associated
of neuronal
with an in-
bodies
as well as with transformations
configurations
prian in-
zones but rather
modification
ters. This would have been crease
through
in these
in the den-
of the postsynaptic
neurons.
NTTOM.
(NSC), thalamo-pretectal NOVT.
NOPC.
A comparison toids indicate tent pattern
species of elasmobranchs
the existence of organization
tem in all selachians.
of a common
firmed by further experimental
studies of other sela-
chian species, both very primitive and highly specialized. In addition, the experimental investigation of the primary visual system in the Hofocephalii regarded as a sister group of the selachians, should make it possible to compare and define organizational aspects of this system which are common to both subclasses. This would provide some indication of the primitive pattern of this system, which was present in
inal projection
and consis-
Many of the discrepancies
ferences
be con-
of selachian
may be listed to methodological
and/or interspecies
ob-
and ba-
of the primary visual sys-
system”‘.
must
tectal
of the data with those previously
tained in different
ported in studies on the organization
this hypothesis
and
(SFGS) levels.
Comparable remarks have been made with regard to the evolution of the actinopterygian primary visual However,
(NODLAT,
NOCpd)
variations
reretdif-
in the cytoar-
chitecture of the different visual centers. Moreover, a comparison of the primary visual system of more primitive squalomorph sharks with that of the more advanced galeomorph sharks and batoids suggests that this system neuronal density formations in the synaptic neurons the total number
evolved through an increase in the of the target structures and transdendritic configurations of the postrather than through an increase in of projection zones.
the ancestral stock of both phyletic groups. SUMMARY
ACKNOWLEDGEMENTS
The retinal projections of the shark Scyliorhinus canicula were investigated using both the degeneration technique after eye removal and the radioautographic method following the intraocular injection of various tritiated tracers (proline, leucine, fucose, adenosine). The results showed contralateral projection via different optic tract components (TOM, AOT, Tom, TOI, ROVm, RODm) to various areas and nuclei of the hypothalamus (NSC), thalamus (NODLAT, NODMAT, NTTOM, NOVT. NODPT), pretectum (NOPC, NOCPd, NOCPV),
We would like to thank the Laboratoire de Biologie Marine du Collkge de France B Concarneau and the Laboratoire d’Anatomie ComparCe (Paris) for use of their facilities. We express our gratitude to Dr. M.H. Du Buit for his advice and support during the course of this research. We also thank M. Amouzou, S. Arnold, F. Roger and G. Sanchez for their technical support, D. Le Cren for his skillful photographic assistance and B. Alvarado-Ellis for improving the English. This work was supported by the INSERM, the CNRS (UA 662), MRT (85.00 349) and CRSNG.
ABBREVIATIONS AOTMD CH CHO CP CT EW FLM FR
Area optica tegmenti mesencephali dorsalis Commissura habenularum Chiasma opticum Commissura posterior Commissura tectalis Nucleus of Edinger-Westphal Fasciculus longitudinalis medialis Formatio reticularis
HAB IC IN IP LIH NLOB NMH NOCPd NOCPdi
Nucleus habenularis Nucleus intercollicularis Nucleus interstitialis Nucleus interpeduncularis Lobus inferior hypothalami Nucleus lobi lateralis Nucleus medius hypothalami Nucleus opticus commissurae posterioris pars dorsalis Ipsilateral nucleus opticus commissurae
247
NOCPv NODLAT NODLATi NODMAT NODPT NOPC NOPCi NOpD NOpG NOTMV NOTMVI NOTMVm NOVT NOVTi NP NPH NSC NT-TOM NTTOMi N III osc ROB RODM ROVM SAC SFGC SFGS
posterioris pars dorsalis Nucleus opticus commissurae posterioris pars ventricularis Nucleus opticus dorsolateralis anterior thalami Ipsilateral nucleus opticus dorsolateralis anterior thalami Nucleus opticus dorsomedialis anterior thalami Nucleus opticus dorsalis posterior thalami Nucleus opticus pretectalis centralis Ipsilateral nucleus opticus pretectalis centralis Right optic nerve Left optic nerve Nucleus opticus tegmenti mesencephali ventralis Lateral part of the nucleus opticus tegmenti mesencephali ventralis Medial part of the nucleus opticus tegmenti mesencephali ventralis Nucleus opticus ventralis thalami Ipsilateral nucleus opticus ventralis thalami Nucleus profundus mesencephali Nucleus periventricularis hypothalami Nucleus suprachiasmaticus Nucleus thalamicus tractus optici marginalis Ipsilateral nucleus thalamicus tractus optici marginalis Nucleus oculomotorius Organon subcommissurale Radix optica basalis Radix optica dorsalis medialis Radix optica ventralis medialis Stratum album centrale Stratum fibrosum et griseum centrale Stratum fibrosum et griseum superficiale
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