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Evidence for refractoriness of the pituitary-gonadal axis to the pineal gland in golden hamsters and its possible implications in annual reproductive rhythms.

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Evidence for Refractoriness of the Pituitary-Gonadal
Axis to the Pineal Gland in Golden Hamsters
and Its Possible Implications in Annual
Reproductive Rhythms ’
RUSSEL J. REITER
Department of Anatomy, The University of Texas Medical School at
Sun Antonio, Sun Antonio, Texas 78229
ABSTRACT
The testes of adult hamsters maintained in short daily photoperiods (1ight:dark [LD] cycles of 1:23, in hours) undergo regression within
ten weeks and spontaneous regeneration within about 30 weeks. Thereafter (at
least up to 80 weeks), as long as these animals are kept in short photoperiods
the gonads do not experience a second atrophic response. After the 30 week
period of dark exposure, if the hamsters are moved into a long photoperiodic
environment (LD 14:lO) for either one or ten weeks and are then returned to
short photoperiods, the gonads do not involute a second time. However, if the
duration of exposure to LD 14: 10 is increased to 22 weeks, the return to LD 1:23
causes the gonads to degenerate. The regressive responses of the testes never
occur in hamsters that have been pinealectomized indicating that the observed
changes are mediated by this gland. The inability of darkness and, thus the
pineal gland, to induce a second gonadal involution unless the hamsters are
maintained in LD cycles of 14:lO for 22 weeks (after a 30 week period of dark
exposure) may be explicable in terms of ( l ) , a transient refractoriness of the
brain to the pineal antigonadotropic principle or ( 2 ) , the temporary failure of
the pineal to be activated by short daily photoperiods.
Most mammals exhibit seasonal variations in sexual activity and competence
(Ortavant et al., ’64; Hafez, ’64; Lodge and
Salisbury, ’70). The annual reproductive
(cycle of a hibernatory species, the golden
hamster (Mesocricetus auratus), has been
studied in detail by Mogler (’58) Smit-Vis
and Akkerman-Bellaart (’67), Czyba (’68)
and by Vendreley et al. (’70). The following is a brief summary of some of the
salient features of the cycle in this species:
a greater percentage of the animals are
sexually fertile during the “summer” than
during the “winter” months; the germinal
epithelium is microscopically inactive during the hibernatory period (winter) and
it is highly active during seasons with increasing or long daily photoperiods (spring
and summer) ; the gonads of hibernating
hamsters begin to regenerate in late January before the emergence of the animals
from hibernation in mid-March; short
daily photoperiods do not prevent the reacANAT. REC., 173: 365-372.
tivation of the gonads in hibernating
hamsters. These seasonal phenomena
occur in both the males and the females
of the species. A similar cycle in the level
of gonadal activity can be experimentally
induced by restricting the amount of light
to which hamsters are exposed. For example, if adult male hamsters are maintained in an environment which provides
only two hours of light per day (Hoffman
et al., ’65) or if they are blinded by bilateral orbital enucleation (Reiter, ’69a),
their testes regress to a non-functional
state; this condition simulates what happens to the gonads of hamsters during the
winter hibernatory state. After 20 to 25
weeks the gonads of light-deprived animals
regenerate to the functionally mature
state; this response is presumably reminiscent of the regrowth phase of the gonads
the hamsters experience in the late stages
Received Dec. 27, ‘71. Accepted Feb. 18, ’72.
1 Supported by U.S.P.H.S.
grant HD-06523.
365
366
RUSSEL J. REITER
(January to mid-March) of hibernation.
In hamsters that are pinealectomized,
darkness or blinding are incapable of inducing atrophy of the reproductive system
(Hoffman and Reiter, ’65; Reiter, ’69a,b).
These interrelationships tempted the investigators to conclude that in hamsters
dark-induced seasonal changes in reproductive activity may involve the pineal
gland (Hoffman and Reiter, ’65; Reiter,
’69a,b). The following study was designed
to further study the interaction of the
environmental photoperiod, the functional
state of the reproductive organs, and the
pineal gland.
MATERIALS AND METHODS
A total of 565 adult male hamsters,
purchased from Lakeview Hamster Colony,
Newfield, New Jersey, were used in these
studies. Throughout the investigation,
animals were maintained in either long
@ght:dark [LD] cycles of 14: 10, in hours)
or in short (LD 1:23) daily photoperiods.
Lighting intensity at the level of the cages
varied from 50 to 170 foot c. Light was
provided by Westinghouse 20 watt “cool
white” (F20T12/CW) fluorescent bulbs.
At various times during the experiment
all animals were either subjected to sham
or real pinealectomy, to superior cervical
ganglionectomy (SCG) or they were
blinded while anesthesized with sodium
pentobarbital. The hamsters were housed
four or five per clear polycarbonate cage
(25 X 45 x 20 cm) and were provided
with Purina rodent chow and water ad
libitum. With only a few exceptions each
experimental group consisted of eight
hamsters. The animals were usually killed
at ten week intervals. At necropsy, the
weights of the testes and accessory sex
organs (seminal vesicles and coagulating
glands) were recorded and all tissues were
fixed in Bouin’s fluid and retained for
histological study. Without exception, the
pattern of degeneration and regrowth of
the accessory sex organs followed that of
the testes. Because of this, the status of
the secondary sex organs will not be discussed in this report but it should be remembered that they exhibited growth
changes similar to those of the gonads.
Data were analyzed using a student “t”
test. Values that differed at the 5% level
of probability were accepted as being significantly different. The experiment was
begun September 15 and the last animals
were killed 82 weeks later.
RESULTS
When hamsters were maintained in long
daily periods of light (LD 14:lO) for the
duration of the experiment, the testes were
invariably grossly (fig. 1A) and microscopically normal. Under these conditions,
the testes of the pinealectomized hamsters
never differed from those of sham operated animals. If non-pinealectomized
hamsters were maintained in LD cycles of
1:23, however, their testes exhibited a
highly significant, although transitory, involution (fig. 1B). The testes had regressed
completely by ten weeks after dark exposure. In the atrophic state the testes
showed pronounced spermatogenic arrest
and the germinal epithelium consisted of
only spermatogonia and Sertoli cells. The
testes regrew to the functionally mature
condition within 30 weeks after exposure
of the animals to the short daily photoperiods (fig. 1B). The recrudescent testes
were microscopically indistinguishable
from those of animals kept in LD cycles
of 14:lO. Thereafter, as long as the
hamsters were kept in LD cycles of 1:23,
the reproductive organs did not undergo a
second decline in weight or a change in
microscopic appearance. The testes of animals subjected to pinealectomy prior to
being subjected to LD cycles of 1:23 never
degenerated (fig. 1B).
Thirty-two animals that had been exposed to LD 1:23 for ten weeks and possessed involuted gonads were returned to
long daily photoperiods. Within ten weeks
the testes of these animals had regrown
to the adult condition (fig. 1C). At this
point, half of the animals were pinealectomized, half were sham operated and all
were returned to an environment which
provided only one hour of light per day.
The testes of these hamsters remained at
the adult size even though the animals
were exposed to near total darkness for
20 weeks.
The testes of animals in LD 1:23 cycles
for prolonged periods undergo a highly
significant involution with a subsequent
regeneration after 30 weeks and there-
367
PINEAL AND SEASONAL RHYTHMS
LD 14:lO
I
I
I
4; I
PX
21-
0
or
SH
A
I
I
I
I
I
I
I
I
LD 1:23
-6-
I
0
10
i
t
/-6--Q'
I
I
I
I
I
I
I
I
20
30
40
50
60
70
80
DURATION OF TREATMENT (WKS)
Fig. 1 Effects of long (LD 14:lO) or short (LD 1 : 2 3 ) photoperiods and of sham (SH)
or real (PX) pinealectomy on the size of the testes of adult male golden hamsters. Each
point represents the mean testicular weight of seven or eight hamsters. Solid points indicate
intact or sham operated hamsters and hollow points indicate pinealectomized animals.
Vertical lines from points signify standard errors.
,after remain at the mature level as long
;as the animals are kept in short daily
photoperiods (fig. 1B). In the following
phase of the experiment, after 30 weeks
of exposure to LD 1 :23 cycles most of the
liamsters with recrudescent gonads were
ireturned to LD cycles of 14:10 for varying
lengths of time, i.e., either one week, ten
weeks, or 22 weeks. After these intervals
of exposure to long photoperiods, the
hamsters were subjected to either real or
sham pinealectomy and were returned to
LD 1 :23 cycles. The gonads of hamsters
ihat were maintained in LD 14:10 for the
one week interval and were then returned
to darkness did not degenerate even in
animals with an intact pineal gland (fig.
2A). Likewise, if they had been in long
photoperiods for a ten week interval the
return to darkness did not initiate gonadal
regression (fig. 2B). However, if hamsters
had been exposed to an interval of long
photoperiods of 22 weeks duration, the
return to LD 1 :23 cycles caused the testes
to involute unless the hamsters had been
pinealectomized (fig. 2C). In this case, the
return to darkness was designed so it
would be exactly one year (52 weeks)
after the onset of the experiment. The
second degeneration of the gonads was
again followed by a regrowth of the testes
within 30 weeks (fig. 2C).
If initially dark-exposed (for 30 weeks)
hamsters were subsequently maintained in
LD 14: 10 cycles for 32 weeks and were
then returned to short daily photoperiods,
those animals with intact pineal glands
experienced a second gonadal involution
(fig. 3A). The importance of photic reception by the eyes was demonstrated by the
following study. When intact hamsters
were kept in darkness for 30 weeks, returned to LD 14:lO cycles and after 22
weeks were blinded (by bilateral orbital
368
RUSSEL J. REITER
11
LD 1:23
lLD 14:IOl
LD1:23
10
B
I
LD l:23
1
.
I
10
I
I
I D 1:23
0
LD 1:23
I D 14:10F
4:
20
30
I
I
I
LD 14:lO
40
I
50
I
I
I
LD 1:23
60
70
80
DURATION OF TREATMENT (WKS)
Fig. 2 Effect of exposure of hamsters to LD 14:lO cycles (after an initial 30 week
period of exposure to LD 1:23) for either one (A), ten ( 3 ) or 22 ( C ) weeks on the subsequent degenerative response of the gonads to short photoperiods. Each point represents
mean testicular weights of six to eight hamsters. Solid points indicate intact or sham
operated hamsters and hollow points indicate pinealectomized animals.
enucleation), the gonads regressed even
though the animals were maintained in
long daily photoperiods (fig. 3B). Finally,
removal of the superior cervical ganglia,
like pinealectomy, prevented testicular
involution both during the first and second
exposure to decreased photoperiodic length
(fig. 3C).
Histologically, all testes that weighed
less than 1200 mg were atrophic; these
changes have been described elsewhere
(Reiter, '69a). The testes of animals that
had undergone degeneration and had subsequently regenerated were morphologically indistinguishable from those of hamsters kept in long photoperiods throughout
the study.
DISCUSSION
The present results confirm an earlier
observation (Reiter, '69a) that continual
light deprivation in hamsters induces a
period of reproductive dormancy which is
followed by regrowth of the gonads within
25 to 30 weeks and that, thereafter, the
reproductive organs remain in a functionally and structurally mature state. The
period (approximately 20 weeks) of reproductive quiescence is presumed to
simulate the winter season in hamsters
under field conditions when their gonads
are also involuted. The spontaneous regeneration of reproductive organs in lightdeprived animals is also reminiscent of
the regrowth of the gonads of hibernating
hamsters near the end of the hibernatory
period ( Smit-Vis and Akkerman-Bellaart,
'67). Hence, it appears that the seasonal
sexual cycle which hamsters in their
natural habitat experience can also be induced in laboratory-maintained animals by
restricting the amount of light to which
the animals are exposed. Wild hamsters,
369
PINEAL AND SEASONAL RHYTHMS
L D 1:23
LD 1:23
u ;-
I
I
LD 1:23
I
LD 1430
I
I
LD 1 4 3 0
I
I
I
I
I
LD14:lO
I
J
LD 1:23
I
I
ILD 1:23j
1-
0
I
0
10
I
I
1
I
I
30
40
50
60
DURATION OF TREATMENT (WKS)
20
1
70
I
80
Fig. 3 Effects of blinding (BL), blinding and pinealectomy (BL + PX) and superior
cervical ganglionectomy (SCG) on the gonads of hamsters kept in either long (LD 14:lO)
or short (LD 1:23) daily photoperiods. Each point represents mean testicular weight of
seven or eight hamsters. Solid points indicate inkact or sham operated hamsters and hollow
points indicate pinealectomized animals. The solid triangle represents blinded hamsters
whereas the hollow triangle represents blinded pinealectomized animals. Hollow squares are
the superior cervical ganglionectomized animals. Vertical lines from the means signify
standard errors.
#of course, enter underground burrows in
the fall prior to the onset of hibernation
and, therefore, are presumably exposed to
‘very similar shortened daily photoperiods
lor, for that matter, perhaps no light
whatsoever.
The idea that the pineal gland, because
{of its functional dependence on the environmental photoperiod, is related to seaisonal reproductive rhythms has been suggested by a variety of anatomical (Negik,
’62; Cuello and Tramezzani, ’69; Elden
et al., ’71) and physiological (Czyba et al.,
’64; Reiter, ’69b) studies. The present
findings lend additional credence to this
suggestion. In particular, the observations
ithat hamsters had to be exposed to long
daily photoperiods for 22 or more weeks
‘(after a 30 week period of short “days”)
before LD 1:23 cycles could induce a
second gonadal regression seems especially
to support this concept. After the period of
sexual dormancy, during the 30 week
period of LD 1 :23 cycles, the animals had
to be exposed to long “days” for a period
of time which presumably was roughly
equivalent in length to their natural breeding season. This 22 week interval of LD
14: 10 cycles presumably simulated the
“summer” months. During this period the
pituitary-gonadal axis is apparently refractory or insensitive to the pineal antigonadotropic influence as evidenced by the fact
that subjecting hamsters to reduced daily
photoperiods during this time failed to
depress their reproductive system. The
alternative explanation is that long periods
of darkness during this period were in-
370
RUSSEL J. REITER
capable of stimulating pineal antigonadotropic activity.
The ability of the brain to “ignore”
photoperiodic influences during selected
periods has a precedent from studies in
which the experimental conditions were
similar to those used here. Seasonal refractoriness of the pituitary-gonadal axis is
particularly common in birds but occurs
in mammals as well. For example, exposure of male English sparrows to long
photoperiods during November served as
a stimulus to the reproductive system
while similar type of treatment in early
August had no stimulatory effect on the
induction of spermatogenic activity (Riley,
’36). Other avian species including the
duck (Benoit et al., ’ 5 0 ) , the junco (Wolfson, ’52), the gold-crowned sparrow
(Miller, ’51) and the starling (Burger,
’47) exhibit refractory periods like those
described by Riley (’36). In mink, Hammond (’51, ’54) claims to have observed
a refractory period of the pituitary-gonadal
axis to a change in the length of the daily
photoperiod. In all species in which a refractoriness of the hypothalamo-pituitary
axis has been observed, it seems to be
manifested at the neural level (Farner,
’71). The mechanism which determine the
refractory periods are, however, poorly
understood.
The period of refractoriness in some
species would preclude the necessity for a
change in pineal activity as a function of
season and may indicate that the functional status of the gonads is determined
merely by the sensitivity (threshold) of
the neuroendocrine axis to exteroceptive
influences. That is, the pineal may be
sufficiently active during all seasons to
induce gonadal involution but only during the winter months is the neuroendocrine axis sensitive to the pineal hormone. It is possible that the threshold of
sensitivity may be adjusted by the ambient
temperature, food availability or other
environmental factors. In that these potential variables were seemingly kept constant
in the present study, the findings indicate
that these factors may not be operative in
the case of the hamster while in other
species they may be of paramount importance (Reiter and Sorrentino, ’71). Another
explanation for the inability of “short days”
to induce a second involution of the reproductive organs (in hamsters that had been
exposed to less than 22 weeks of LD 14: 10
cycles after 30 weeks of LD 1:23 cycles)
may be related to the failure of darkness
to stimulate the antigonadotropic capability of the pineal gland. This explanation
implies, in essence, that the pineal is “exhausted’ after 30 weeks of darkness and
that it requires approximately 22 weeks in
long photoperiods to “regenerate” its capability. The exhaustion hypothesis seems to
be the least likely of the two explanations.
For example, it does not suffice to explain
the failure of “short days” to induce decremental changes in the gonads of hamsters
that had previously been exposed to only
ten weeks of LD 1:23 cycles (during which
testicular degeneration ensued) followed
by ten weeks of LD 14 :10 cycles (during
which the gonads regenerated) (fig. 1C).
This latter finding would be most readily
explicable in terms of a refractory period
as well.
LITERATURE CITED
Benoit, J., I. Assenmacher and F. X. Walter
1950 RCsponses du mCchanisme gonadostimulant a l’bclairement artificiel et de la
prkhypophyse aux castrations bilaterale et unilatkrale, chex le canard domestique male, a u
cours de la pkriode de regression testiculaire
saisonnierh. C. R. SOC. Biol. (Paris), 144:
573-577.
Burger, J. W. 1947 On the relation of daylength of the phases of testicular involution
and inactivity of the spermatogenic cycle of
the starling. J. Exp. Zool., 105: 259-267.
Cuello, A., and J. Tramezzani 1969 The
epiphysis cerebri of the Weddell seal: its remarkable size and glandular pattern. Gen.
Comp. Endocr., 12: 154-164.
Czyba, J. C. 1968 Les fluctuations de la
fCcondit6 chez l e Hamster dor6 (Mesocricetus
auratus Waterhouse) au C O U ~ S de l’annee.
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Czyba, J. C., C. Girod and N. Durand 1964 Sur
I’antagonisme bpiphyso-hypophysaire et les
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chez le Hamster dore (Mesocricetus auratus).
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Elden, C. A., M. C. Keyes and C. E. Marshall
1971 Pineal body of the northern f u r seal
(Callorhinus ursinus): A model for studying the
probable function of the mammalian pineal
body. Amer. J. Vet. Res., 32: 639-647.
Farner, D. S. 1961 Comparative physiology:
photoperiodicity. Ann. Rev. Physiol., 23: 71-96.
Hafez, E. S . E. 1964 Environment and reproduction in domesticated species. Int. Rev. Gen.
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PINEAL AND SEASONAL RHYTHMS
Hammond, J., Jr. 1951 Control by light of reproduction in ferrets and mink. Nature
(London), 167: 150-151.
1954 Light regulation of hormone
secretion. Vit. Horm., 12: 1.57-206.
Hoffman, R. A., R. J. Hester and C. Townes
1965 Effect of light and temperature on the
endocrine system of the golden hamster (Mesocricetus auratus Waterhouse). ComD. Biochem.
Physiol., 15: 525-533.
]Hoffman, R. A., and R. J. Reiter 1965 Pineal
gland: Influence on gonads of male hamsters.
Science, 148: 1609-1611.
]Lodge, J. R., and G. W. Salisbury 1970 Seasonal variation and male reproductive efficiency. In: The Testes. Vol. 3. A. D. Johnson,
W. R. Gomes and N. L. VanDemark, eds.
Academic Press, New York, pp. 139-167.
Miller, A. H. 1951 Further evidence on the
refractory period in the reproductive cycle of
the golden-crowned sparrow, Zonotrichia coronata. Auk, 68: 380-383.
Illogler, K.-H. 1958 Das Endokrine System des
Syrischen Goldhamster unter Berucksichtizung
des Naturlichen und Experimentellen Winterschlaf. 2. Morphol. Oekol. Tiere, 47: 367-408.
Nesic, Lj 1962 Contribution B l'dtude du
rhythme saisonnier de la glande pineale de
brelus. Acta Anat., 49: 376377.
Ortavant, R., P. Mauleon and C. Thibault 1964
Photoperiodic control of gonadal and hypoph-
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yseal activity in domestic animals. Ann. N.Y.
Acad. Sci., 217: 157-192.
Reiter, R. J. 1969a Pineal function in long
term blinded male and female golden hamsters.
Gen. Comp. Endocr., 12: 460-468.
1969b Pineal-gonadal relationships in
male rodents. In: Progress in Endocrinology.
C. Gual, ed. Excerpta Medica Fdn., Amsterdam,
pp. 631-636.
Reiter, R. J., and S. Sorrentino, Jr. 1971 Factors influential in determining the gonadinhibiting activity of the pineal gland. In: The
Pineal Gland. G. E. W. Wolstenholme and
J. Knight, eds. J. and A. Churchill, London,
pp. 329-344.
Riley, G. M. 1936 Light regulation of sexual
activity in the male sparrow. Proc. SOC.Exp.
Biol. Med., 34: 331-332.
Smit-Vis, J. H., and M. A, Akkerman-Bellaart
1967 Spermiogenesis in hibernating golden
hamsters. Experientia, 23: 844-845.
Vendrely, E., C. Buerillot, C. Basseville and
C. Da Lage 1970 Relation entre les donnees
histometriques et le poids testiculaire au cours
du cycle saisonnier chez le Hamster dorC. C. R.
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fat cycles of the junco. J. Exp. Zool., 121: 311325.
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