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Premitotic DNA synthesis in the brain of the adult frog Rana esculenta L.An autoradiographic 3H-thymidine study

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THE ANATOMICAL RECORD 228:461-470 (1990)
Premitotic DNA Synthesis in the Brain of the
Adult Frog (Rana esculenta L.): An
Auto radiographic 3H-Thy midine Study
Department of Animal Biology, University of Pavia, The Center for Histochemistry of
Italian National Research Council, Pavia, Italy (G.B., E.S., S.G.); Institute of Physiology,
Czechoslovak Academy of Sciences, Prague, Czechoslovakia (V.M.)
Replicative synthesis of DNA in the brain of the adult frog was
studied by light microscope autoradiography. Animals collected during the active
period (MayJune) and in hibernation (January) were used. In active frogs, 3Hthymidine labelling occurred mainly in the ependymal cells which line the ventricles. The mean labelling index (LI%)was higher in the ependyma of the lateral
and fourth ventricles than in the ependyma of the lateral diencephalon and tectal
parts of the mesencephalon. In the recessus infundibularis and preopticus the
number of labelled cells (LCs) was several times greater than in the lateral parts
of the third ventricle. LCs were seen subependymally only occasionally. The incidence of LCs in the parenchyma of the brain was much lower in most regions than
in the ventricular ependyma; LCs were mainly small and, from their nuclear
morphology, they were glial cells. The LI% reached the highest value in the septum hippocampi and in the nucleus entopeduncularis. In these locations, LCs were
larger and closer in size to the nerve cells of these regions. From comparison with
data obtained earlier in the brain of mammals, it is evident that the distribution
of proliferating cells in the olfactory and limbic system is phylogenetically conservative. The occurrence of pyknotic cells in the same areas which contain LCs,
suggests that cell division reflects in part the process of cell renewal observed in
mammals. However, proliferating cells could also be linked to the continuous
growth observed in non-mammalian vertebrates. In hibernating frogs, LCs and
pyknoses were not seen or were found occasionally, which further indicates the
functional significance of both processes.
Several studies have reported cell division in discrete
brain regions of non-mammalian vertebrates (Kirsche,
1967; Kranz and Richter, 1970a, 1970b; Richter and
Kranz, 1970a, 1970b, 1971; Polenov et al., 1972;
Chetverukin, 1978; Raymond and Easter, 1983; LopezGarcia et al., 1988; Yanes Mendez et al., 1988). From
these studies, it appears that cell proliferation in the
brain of non-mammals differs substantially from that
in mammals (Smart and Leblond, 1961; Altman, 1963,
1966,1969; Altman and Das, 1964; Dalton et al., 1968;
Hommes and Leblond, 1969; Kaplan and Hinds, 1980;
Korr, 1980; Mares, 1986). The main difference appears
to be in the proliferation of ependymal cells, both under
normal conditions and during healing andlor repair. In
contrast to mammals, a part of the ependyma in the
adult brain of most non-mammalian vertebrates retains its matrix character, which can be activated after
damage (Kranz and Richter, 1971). The residual matrix is distributed unevenly along the brain ventricles
and, as shown in Teleostei by 3H-thymidine autoradiography (Kranz and Richter, 1970a, 1970b; Richter
and Kranz, 1970a, 1970b, 1971), it is expressed at a
similar, though low, level for most of the animal's life.
Proliferation of cells in the subependymal regions,
which is considerable in some parts of the mammalian
brain, is much lower (Kirsche, 1967; Fleischauer, 1972;
Polenov et al., 1972). The residual cell proliferation,
resulting in long-lasting formation of new nonneuronal and probably neuronal cells, leads to continuous growth of the brain and increase in the total cell
number in Teleostei (Raymond and Easter, 1983).
Much less is known about proliferation of more differentiated cells in the brain parenchyma of adult nonmammals. According to autoradiographic studies performed mainly on fishes, cell division occurs in a small
number of parenchymal glial cells (Kranz and Richter,
1970a, 1970b; Richter and Kranz, 1970a, 1970b, 1971;
Reznikov, 1981; Raymond and Easter, 1983) and perhaps in neurons of some brain regions, e.g., cerebellum
and optic tectum (Rahmann, 1968; Raymond and Easter, 1983).
Received October 17, 1989; accepted April 27, 1990.
Address reprint requests to Prof. Dr. Graziella Bernocchi, Dipartimento di Biologia Animale, Laboratorio di Istologia, Piazza Botta 10,
27100 Pavia, Italy.
TABLE 1. Distribution of mean labelling index (LI%)in different
brain regions of adult frogs during active period
Brain vesicles
Lateral ventricles (E)
Bulbus olfactorius (P)
Pallium mediale (P)
Pallium dorsale and laterale (P)
Septum hippocampi (P)
I11 ventricle (E)
Recessus preopticus (E)
Recessus infundibularis (E)
Nucleus entopeduncularis (P)
Tectum ventricle (E)
Aqueductus Silvii (E)
Tectum opticum (P)
IV ventricle (E)
Cerebellum (P)
Medulla oblongata (P)
LI% (2s.d.)
1.33 2 0.45
0.65 i 0.56
0.15 f 0.25
3.72 f 0.54
0.17 2 0.15
0.92 & 0.31
1.86 2 0.09
15.32 3.18
0.20 2 0.28
0.18 t 0.25
1.47 2 0.50
0.19 & 0.32
0.86 f 0.35
Abbreviations: E, ependymal layer; P, parenchyma.
The data available so far do not provide a complete Processing and Evaluation of Labelled and Pyknotic Cells
picture of the rate of cell proliferation within the whole
After killing, the brains were removed immediately
brain, especially of amphibians. A more complete de- and fixed in Carnoy solution (6:3:1) for 12 hours. Hisscription is necessary for comparison of this process in tological sections (4 pm thick) of paraffin-embedded
phylogenetically distant species. This could help t o re- whole brains were cut in the sagittal and transverse
veal evolutionary links in residual cell proliferation planes. The slides were covered with Kodak ARlO
and its possible functional significance in the brain of Stripping Film and exposed for 10-14 days. With this
adults. Similarly, the morphology of cells engaged in exposure time, well-labelled cells were obtained with a
premitotic DNA synthesis needs further specification. reasonably low background. Evaluation was performed
Further, the occurrence of cell death, normally present on toluidine blue stained autoradiograms. Cells were
in mammalian nervous system (Sturrock, 1979; Pan- considered as labelled when a t least 10 silver grains
nese, 1981) has not yet been documented for non-mam- were present over their nuclei, though the majority of
malian vertebrates.
the LCs were heavily labelled (more than 40 silver
This situation, together with our earlier pilot obser- grains).
vations of DNA synthesis in a group of neuron-like
Approximately one section out of each three to ten
large cells in certain parts of the frog brain (Bernocchi (proportionally to the size of the brain region) was evalet al., 19851, have led us: 1)to study more systemati- uated per animal. The total numbers of LCs and unlacally in this species the cell proliferation in ventricle belled cells were counted by scanning a t a magnificalining and brain parenchyma by pulse 3H-thymidine tion of ~ 1 , 0 0 0around the ventricles and in the
autoradiography; 2) to compare data from animals dur- parenchyma of individual brain regions separately.
ing active period and winter inactivity; and 3) to inves- The labelling index (LI%) was calculated as the pertigate the relationship between the frequency of la- centage of LCs in respect to the total number of cells in
belled cells (LCs) and that of pyknotic cells in the two the individual brain regions. The LI% values (Table 1)
periods of the frog annual cycle.
were calculated as mean values from the means (-t s.d.)
measured in individual animals. The drawings of the
distribution of LCs (Figs. 1,2) were obtained from four
superimposed sections of one representative active
Experiments were carried out with adult frogs (Rana frog. The evaluation of the frequency of pyknotic cells
esculenta L.) of about 7 cm length (legs excluded), col- was limited to the areas with the highest or the lowest
lected in their natural environment in May and June LI% in active animals. The hematoxylin eosin stained
(20-25"C), i.e., during the period of activity, and kept specimens were used to distinguish these cells from
in the laboratory for 1 month before the experiment. erythrocytes.
Other animals were collected in January (0-5"C), during underground hibernation, and used immediately.
The animals (six specimens for the active period and
four for hibernation) were injected with 5 pCi/g body
3H-Thymidine Incorporation
weight of 3H-thymidine (specific activity 865 GBq/
mM, UVVVR, Prague) in the inguinal lymphatic sac
and killed by decapitation 2 hours later. After injection Active frogs
The distribution of 3H-thymidine LCs in different
both active and hibernating animals were kept a t room
temperature (23°C). Animals without injections (three regions of the frog brain is schematically shown in Figspecimens for the active period and two for hiberna- ures 1, 2. The majority of the DNA-synthesizing cells
tion) were used for morphological description and were heavily labelled. Their incidence and cytological
characteristics will be given below.
counting of pyknotic cells.
Regional differences in DNA synthesis of ependymal cells.
The brain ventricles of R. esculenta are lined by
ependymal cells similar to those described by Paul
(1967) for Rana temporaria. The main cell types are
unipolar and bipolar tanycytes (gliocytes). Unipolar
tanycytes show a central nucleus and cytoplasm reduced to a thin rim towards the ventricle lumen, while
bipolar tanycytes have an eccentric nucleus. In some
places cells of the wedge-shaped ependymal type (columnar tanycytes), i.e., the “Furchenependym” of Paul
(1967), are found. Regressive modified ependymal cells
(epithelial cells) with flat nuclei close to the ventricles
are also present. In general, LCs were mainly ependymal. Subependymally, LCs were seen only occasionally. Because of the small number of labelled
subependymal cells, quantitative evaluation of LCs
was done only for proper ependymal cells.
Regional differences in DNA synthesis in the brain parenchyma. In most of the brain parenchyma LCs were rare
(Table 1).They were numerous (LI% 3.72) in the nuclei
of septum hippocampi (Fig. 5A,B), which are located
dorsally, near the meningeal envelopes. These nuclei
consist of cells which resemble neurons. They are of
medium size with roundish nuclei, in which chromatin
is packed in small clumps. Some of these cells were
labelled quite heavily. In the pallium dorsale and laterale, there were few or no LCs. However, in the remaining pallium mediale (primordium hippocampi),
LCs occurred more frequently (LI%0.15) and they were
similar t o nerve cells in size. LCs were also scattered in
the bulbus olfactorius (LI% 0.65).
There was a cluster of LCs (LI% 15.32) near the preoptic area (Fig. 5C,D). In this location, which corresponds to the nucleus entopeduncularis, LCs were
large, with a pale and roundish nucleus.
1. The telencephalic ventricles are lined mainly by a
Inside the cerebellum, there were few LCs (LI%
monostratified ependyma; dorsally and ventrally, 0.19). The cells were small and located mainly in deep
pluristratified ependyma can be found. Ependymal parts of the internal granule layer. LCs were very rare
cells of the lateral ventricles are mainly unipolar tany- in the mesencephalic tectum (<0.01%).
cytes. Dorsally, there are bipolar tanycytes and, both
LCs were also present in the parenchyma of the medorsally and ventrally, some wedge-shaped ependymal dulla oblongata (LI% 0.86) and they appeared to be
cells are present.
LCs were mainly unipolar tanycytes. An average
Brain accessories. In all locations, endothelial cells or
LI% was 1.33 (Table 1).LCs were not evenly distrib- cells accompanying blood vessels were occasionally lauted. The highest frequency of LCs was found in the belled. LCs frequently occurred in the choroid plexi of
ventral and medial parts of the ventricular wall (Fig.
3A,B), especially at the middle of the anterior-posterior
axis of the telencephalon. The DNA-synthesizing cells
occurred often in pairs or small clusters.
2. In the diencephalon, ependymal cells are mono- AMY
aqueductus Sylvii
stratified laterally and pluristratified in the recessus AS
bulbus olfactorius
preopticus. Laterally, the ependymal lining is formed BO
by unipolar tanycytes and, only dorsally, by regressive CH
chiasma opticum
modified ependymal cells. In some places subependy- GL
glomerula olfactoria
granular layer
ma1 cells are present. The ependymal cells of the reces- GR
sus preopticus and recessus infundibularis are mainly HA
unipolar tanycytes; bipolar tanycytes and regressive INF
lateral ventricle
ependymal cells occur occasionally in these localities. MI
layer of mitrial cells
nucleus accumbens septi
The mean LI% (Table 1) for the lateral parts of the NAS
nucleus centralis thalami
third ventricle was low (0.17) and the LCs were mainly NCT
nucleus dorsalis septi
of the unipolar tanycyte type; some labelled regressive NDS
nucleus entopeduncularis
ependymal cells were also found. In the recessus pre- NID
nucleus infundibularis dorsalis
nucleus interpeduncularis
opticus and in the recessus infundibularis (Fig. 4A,B), NIS
nucleus infundibularis ventralis
LCs were mainly unipolar tanycytes. The LI% values NIV
nucleus lateralis thalami
in the latter two regions (0.92 and 1.86) exceeded by NMS
nucleus medialis septi
several times the values for the lateral parts of the NPT
nucleus posterior thalami
nucleus princeps tori semicirculari
third ventricle. In the recessus preopticus some la- NPTS
nucleus ventromedialis thalami
belled bipolar tanycytes were found. Occasionally LCs NVMT
plexus choroideus
were also found subependymally near both recesses.
pallium dorsale
3. In the mesencephalon, the tectal ventricle and the PG
pretectal gray
pallium laterale
aqueductus Silvii are covered mostly by monostratified PL
pallium mediale
ependyma formed by unipolar tanycytes; in the dorsal PM
preoptic recessus organ
part of the aqueduct, some wedge-shaped cells occur.
paraventricularis organ
The LI% values (Table 1)were low (0.20 and 0.18) in RI
recessus infundibularis
substantia grisea centralis
both locations (Fig. 3C,D).
septum hippocampi
4. In the metencephalic ventricle, the lateral SSTH
ependyma appears pluristratified. The cells are unipo- TEO
tectum opticum
lar tanycytes and regressive ependymal cells. Ven- TO
tractus opticus
ventricula tecti
trally, some of the ependymal cells are wedge-shaped. VT
nucleus nervi trigemini
The LI% amounted to 1.47 (Table 1); LCs were V
nucleus of the 6th nerve
mainly of regressive type. In the ventral regions, mi- VII
nucleus motorius nervi facialis
toses were observed.
nucleus vestibularis
Fig. 1. Schematic drawings of transverse sections through frog brain
taken at different levels in the rostra1 (A) to caudal (R) direction as
illustrated by the drawing at the right lower side. The distribution of
3H-thymidine LCs is shown in the ventricular wall and the parenchyma. Each triangle indicates the presence of one LC; a black dot
corresponds to three LCs. For each level, four sections from one representative animal were superimposed. A,B,C,D,E,F,G,H telencephalon; I: telencephalon-diencephalon;J,K: diencephalon; L,M: dien-
cephalon-mesencephalon; N,O: mesencephalon; P,Q: metencephalonmielencephalon; R mielencephalon. LCs were highly frequent in C:
the ventricle lining of the telencephalon, in F , G the recessus preopticus, and in M: the recessus infundibularis. Several LCs are present
in E,F: the nuclei of septum hippocampi and in E, F, G the nucleus
entopeduncularis. LCs frequently occur in I,O,Q,R the choroid plexi,
and in E,F,J the leptomeninges. Scale bar = 1 mm.
each ventricle (Fig. lI,Q,R), both in the stromal and the
epithelial compartments. In the leptomeninges, LCs
appeared mainly on the surface of the ventral part of
the brain, especially in its more anterior parts (Fig.
Hibernating frogs
Histologically, no gross differences from active animals were noticed, although the cellular regions adjacent to the recessus preopticus and infundibularis
tended to be smaller.
1.3%, in the septum hippocampi 2.3%, in the nucleus
entopeduncularis lo%, in the recessus preopticus 0.6%,
and 1.5%in the lateral ventricles. During hibernation,
the number of pyknotic cells decreased several fold in
all regions. In the lateral ventricles, they were 0.1%
and in the pallium mediale 0.5%. In the other regions,
in which even higher values were found in active animals (septum hippocampi, nucleus entopeduncularis),
there were practically no pyknotic cells.
Topological and Cytological Comments
Fig. 2. Schematic drawings of sagittal sections through one half frog
brain taken at different levels in A the lateral to D: the medial
direction. The distribution of 3H-thymidine LCs is shown in the ventricular wall and the parenchyma. Each triangle indicates the presence of one LC; a black dot corresponds to three LCs. For each level,
four sections from one representative animal were superimposed.
Note the high frequency of LCs in the ventricle lining of A,B: the
telencephalon and D in the nuclei of septum hippocampi. Scale bar =
1 mm.
In comparison to active animals, LCs were much
fewer in both ventricular and extraventricular regions;
in the latter, no LCs were found in most sections and
isolated LCs were observed only in the ependymal regions. Because of the very small number of the LCs, no
quantitative comparison of labelling differences could
be done.
Pyknotic cells in active and hibernating animals. Cells
with highly basophilic round or irregular nuclei with a
thin rim of hypereosinophilic cytoplasm, typical of cells
undergoing spontaneous death but different than
erythrocytes, were seen. During the active period, the
frequency of pyknotic cells in the pallium mediale was
The location of 3H-thymidine LCs and sporadic mitoses indicates that proliferation of cells in adult frog
brain takes place mainly within the ependymal lining.
This is similar to adult fishes, other amphibians, and
reptiles (Kirsche, 1967; Kranz and Richter, 1970a,
1970b;Richter and Kranz, 1970a, 1970b, 1971; Polenov
et al., 1972; Chetverukhin, 1978; Lopez-Garcia et al.,
1988; Raymond and Easter, 1983; Yanes Mendez et al.,
1988), while in mammals the ependyma is mitotically
less active. For instance, in the forebrain ventricles of
the adolescent rat, the mean LI% is 0.34 (Chauhan and
Lewis, 1979). As in frogs, the values for the third ventricle of rats were much lower (0.03%, Chauhan and
Lewis, 1979). As shown in this study, the incidence of
LCs also varies greatly along the ventricular border of
the frog brain. The higher mean LI% values observed
in the hypothalamic recessus preopticus and infundibularis and in the telencephalic ventricles are on the
whole in agreement with earlier autoradiographic data
obtained for some species of Teleostei (Kranz and Richter, 1970a, 1970b). In contrast to Teleostei, we found
fewer LCs in the tectal and metencephalic ventricles of
frogs. Cytological classification of LCs by light microscope autoradiography is limited. Nevertheless, it
seems apparent that they are mostly tanycytes (gliocytes) of unipolar type. DNA synthesis in bipolar tanycytes has been observed in the hypothalamic preoptic
recessus and in regressing types of ependymal cells in
the diencephalic and metencephalic ventricles. Subependymally, LCs are much rarer. This is in accord
with the very limited amount of subependymal matrix
in non-mammals (Kirsche, 1967; Fleischauer 1972)
and is in contrast to some parts of the mammalian
brain. In mice and rats, where the residual subependyma1 layer is clearly visible near the lateral wall of the
forebrain ventricles (Smart, 1961; Paterson et al.,
1973), the average LI% is 15% to 20% (Smart and Leblond, 1961; MareS, 1975, 1986).
The present study has shown that LCs also occur in
the differentiated parenchyma of the adult frog brain.
Their incidence in some regions, such as pallium mediale and medulla oblongata (0.15% and 0.86%, respectively) is comparable to that observed in mice (Mare6
and Lodin, 1974; Mares et al., 1975). The incidence of
LCs in the cerebellum of frogs is close to the values
observed in other regions (0.19%), while in mice it is
several times lower (Mares, 1975, 1986). A relatively
high incidence of LCs occurs in some parts of the hippocampal and olfactory systems, especially in the septum hippocampi and in the nucleus entopeduncularis;
in the latter the LI% greatly exceeded those of all other
regions of the brain (15.32%). It is noteworthy that
both of these regions are derivatives of the ventral and
Fig. 3
Fig. 4. Photomicrographs of 3H-thymidine labelling in the ventricular wall. A,B: Transverse sections
through the diencephalic recessus infundibularis. 3H-thymidine LCs are mainly located in the ependyma1 cell lining. B: A magnification showing one subependymal LC (arrow). Toluidine blue staining. Bars:
100 pm (A) and 20 pm (B).
medial germinative zones of the telencephalon, in
which residual proliferation in ependyma prevails over
the dorsal zone in amphibians still at adult period of
life. It is of interest that the corresponding homologous
regions in mammalian brain (septum hippocampi, striatal complex) also show relatively active proliferation
(Altman, 1966, 1969; Mareg and Lodin, 1974).
In most other parenchymal regions, LCs were relatively small and appeared t o be glial cells; the LCs in
the nucleus entopeduncularis were larger and looked
like neurons. Also, in the septum hippocampi LCs
Fig. 3. Photomicrographs of 3H-thymidine labelling in the ventricular wall. A,B Transverse section through the middle telencephalon.
A Note the numerous 3H-thymidine LCs (mainly unipolar tanycytes)
in the ependymal lining of the ventral part of the lateral ventricle. B
Higher magnification of a detail in A. Some LCs are clearly visible in
the ependymal lining. C,D: Transverse sections through the mesencephalic aqueductus Sylvii. In the ependymal lining of this localization LCs are much less numerous than in the ependyma of lateral
ventricles. D: Higher magnification of a detail in C showing one 3Hthymidine LC in the ependymal lining. Toluidine blue staining. Bars:
100 pm (A,C) and 25 pm (B,D).
might be neurons. Final classification of these cells is
not possible in our material. Because of the pulse labelling schedule of our experiments, it is clear that
labelling of neuron-like cells in our material is not due
to migration of newly formed neurons from the adjacent germinative zones as described in non-mammalian vertebrates (Polenov et al., 1972; Raymond and
Easter, 1983; Lopez-Garcia et al., 19881, or even some
mammals (Kaplan and Bell, 1983).
Finally, it should be pointed out that in the frog, as
in mammals (MareS, 1986), LCs often occur in groups
or patches of different size. This might be a consequence of repeated divisions of perennially active, or
activated postmitotic cells.
Functional and Comparative Comments
The impact of cell division on number of brain cells
in adults is not fully understood for any of the species
studied. Cell division has been attributed mainly to cell
renewal. Renewal of glial cells has been described in
mice and rats (Korr, 1980; MareS and Lisy, 1980,1983),
and in sexually mature monkeys (Eckenhoff and Rakic,
1988). We admit that cell division in the frog brain
Fig. 5
reflects cell renewal, especially in the regions in which vak Academy of Sciences and partially supported by
the 3H-thymidine LI% is high and, at the same time, the Italian MURST and C.N.R. grants to G.B.
pyknotic cells are present (Sturrock, 1979). However,
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Gaze, 1972). The cell proliferation observed in our
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This work is a part of the scientific joint program
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Italian National Research Council and the Czechoslo-
Fig. 5. Photomicrographs of 3H-thymidine labelling in the brain
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