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Dipartimento di Biologia, Università di Ferrara, Ferrara 44100, Italy
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ABSTRACT |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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To establish whether the capability of daily melatonin injections to entrain circadian rhythms varies with season, we examined in constant conditions the locomotor behavior of lizards Podarcis sicula collected and subjected to daily melatonin injections at different times of the year. Although in summer locomotor rhythms of both pineal-intact and pinealectomized lizards became entrained to the 24-h injection period, in the other seasons their rhythms did not entrain to the injection period. To establish whether the suprachiasmatic nuclei (SCN) mediate summer entrainment of locomotor rhythms to melatonin, we examined the behavioral effects of daily melatonin injections in lizards subjected to either bilateral (SCN-X) or unilateral (USCN-X) ablation of the SCN. SCN-X lizards became behaviorally arrhythmic, and daily melatonin injections did not restore rhythmicity. USCN-X lizards remained rhythmic, and their locomotor rhythms did entrain to the injections. Besides demonstrating for the first time in a vertebrate that daily melatonin injections are capable of entraining circadian rhythmicity in only one season (summer), the present results support the view that the SCN (and not the pineal gland) are the primary target sites of melatonin in the circadian system of P. sicula.
suprachiasmatic nuclei; pineal gland; electrolytic lesions
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INTRODUCTION |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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THE CORE OF THE CIRCADIAN SYSTEM of lizards resides in
three structures of diencephalic origin: the pineal gland, the retinas, and the suprachiasmatic nuclei of the hypothalamus (SCN) (23, 35). In
some iguanid lizards, such as Anolis
carolinensis, Sceloporus occidentalis, and Iguana
iguana, the isolated pineal gland cultured in vitro
synthesizes melatonin with a circadian rhythm, which persists for
several cycles in constant conditions (20, 21, 29). This demonstrates
the existence of circadian oscillators in the pineal gland that are
coupled to melatonin synthesis. Pinealectomy abolishes circadian
rhythms of locomotor activity in A. carolinensis and Gallotia
galloti or induces marked changes in the free-running period of locomotor rhythms (
) and/or the length of
circadian activity (
) in S. occidentalis, Sceloporus
olivaceus, and Podarcis sicula (6, 14, 24, 31-33). In I. iguana pinealectomy abolishes the internally generated
circadian rhythm of body temperature, whereas that of locomotor
activity remains unaffected (30). Several findings in lizards support
the contention that pineal oscillators transmit their circadian
information to the rest of the system hormonally, via rhythmic
secretion of melatonin into the bloodstream. Daily 12-h melatonin
infusions that in S. occidentalis closely mimic the normal, rhythmic pattern of pineal melatonin secretion in this species entrain locomotor rhythms of both
pineal-intact and pinealectomized lizards (12). In P. sicula, either pinealectomy or chronic administration
of exogenous melatonin (in Silastic capsules) suppresses circadian
rhythms of blood-borne melatonin and alters circadian locomotor
behavior in the same way by lengthening , shortening , and
abolishing the bimodal locomotor pattern, when present (6, 9, 10, 14).
Transplantation of a pineal gland from a donor P. sicula into the cerebral interhemispheric fissure of a
pinealectomized lizard produces a sudden, drastic change in in the
host (7).
The retinas of lizards can participate in circadian function not only
as photosensory input to the clock, but also as loci of circadian
oscillators; in I. iguana the retina
isolated in culture drives circadian rhythms of melatonin synthesis
(29). Bilateral ocular enucleation under constant bright light (LL) was
found to induce a marked shortening in in S. olivaceus and S. occidentalis and in some cases arrhythmicity in
S. olivaceus (32, 37). Bilateral
retinalectomy induces a marked shortening in in P. sicula kept in constant darkness (DD), and electrolytic lesions of both optic nerves at the level of the optic chiasm in DD
produce the same behavioral effects as bilateral retinalectomy (6, 22).
This demonstrates that the influence of the retinas on the circadian
system is neurally mediated and independent of light perception.
Whether the SCN of lizards actually contain circadian oscillators is at
present unknown. There are data, however, that indirectly support the
hypothesis that the lizard SCN may contain a primary oscillatory system
that drives behavioral rhythmicity: electrolytic lesions to the SCN
were found to invariably abolish circadian rhythms of locomotor
activity both in Dipsosaurus dorsalis and P. sicula (16, 23).
The three components of the circadian system (pineal gland, retinas, and SCN) are believed to interact with one another and function together as a compound circadian pacemaker (23, 35). The retinas can act neurally on the SCN through a monosynaptic retinohypothalamic pathway (3, 15). In birds, plasma melatonin rhythms of pineal origin were shown to influence SCN activity: the SCN of the house sparrow (Passer domesticus) express circadian rhythms in 2-[125I]iodomelatonin high-affinity binding, which are suppressed by pinealectomy and restored by melatonin administration (17, 18). This provisionally suggests that the behavioral effects of pinealectomy reported in lizards may be due to the abolition of such a melatonin pathway, although evidence for the existence of melatonin receptors within the SCN is still lacking. Remarkably, however, the concentration of melatonin receptors in the neural tissue of the iguanid lizard A. carolinensis was found to be higher than in species belonging to every other class of vertebrates (26).
Progress in understanding how the pineal gland,
retinas, and SCN interact with one another as a compound pacemaker in
P. sicula is made difficult by the
discovery that the role played by the pineal gland in circadian
organization varies with season (13). Changes in in response to
pinealectomy were found to be greater in summer than in all other
seasons, and changes in in response to the same surgery were
detected only in spring and summer. Furthermore, although pinealectomy
is effective in altering dramatically the locomotor rhythms of all
individual lizards tested in summer, the same surgery leaves locomotor
rhythmicity of many lizards tested in autumn and winter completely
undisturbed (13). This suggests the possibility that the target sites
of melatonin within the circadian system of P. sicula undergo seasonal changes in responsiveness to
melatonin secreted by the pineal gland into the blood.
The present experiments were aimed at testing whether daily injections of exogenous melatonin were capable of entraining circadian locomotor rhythms of P. sicula in some seasons and not in others. For this purpose, we examined in constant temperature and DD the locomotor behavior of lizards collected and subjected to daily melatonin injections at different times of the year. Further experiments tested whether the SCN of P. sicula are the target sites of melatonin that mediate entrainment of locomotor rhythms to daily melatonin injections. We compared in constant temperature and DD the behavioral effects of daily melatonin injections in two different groups of lizards, one of which underwent bilateral ablation of the SCN (SCN-X) and the other which underwent unilateral ablation of the SCN (USCN-X). This investigation was carried out in summer, because the results of the seasonal experiments showed that in all other seasons daily melatonin injections do not affect circadian locomotor behavior.
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MATERIALS AND METHODS |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Animals and Locomotor Recording
Ruin lizards P. sicula campestris De Betta 1857 (adult males only, 6.5-8 cm snout-vent length) from the area of Ferrara (Italy) were used. Different groups of P. sicula were collected in November through December 1995, April 1996, July through August 1996, and February 1997. After capture, each lizard was carried to the lab and immediately put into an individual tilt cage (30 × 15 × 11 cm) for locomotor recording. Tilt cages were placed inside environmental chambers kept in constant darkness (DD) and constant temperature (29°C) and were connected to a computer-based data acquisition system (DataQuest III, Mini-Mitter, Sunriver, OR) for monitoring locomotor activity. Food (Tenebrio molitor larvae) and water were supplied twice a week.Melatonin Injections
Lizards were injected subcutaneously every 24 h at the same time of day with 3 µg of melatonin (Sigma, St. Louis, MO) in 10 µl of 1% ethanolic solution or with vehicle solution (10 µl 1% ethanolic solution). The injections were performed under dim red light (50 mW/m2).Surgeries
All surgeries were always performed during the lizard's subjective day (0-12 h after activity onset). For anesthesia, the lizards were first cooled in a refrigerator (1-4°C) for 30-50 min until immobilized. They were then packed in crushed ice and mounted in a Kopf 900 small stereotaxic instrument. Pinealectomy (Pin-X) was performed as described in Foà (6). For electrolytic lesions, an electrode was used that consisted of a platinum-iridium wire (0.05 mm diameter) insulated with teflon (0.075 mm outer diameter) (Advent Research Materials). The direct current supplied to perform the lesions was 0.6 mA for 8-10 s. Bilateral electrolytic lesions to the SCN were performed as described in Minutini et al. (23). For bilateral lesions (SCN-X), lesion coordinates were as follows: 0.00 mm lateral and 0.8 mm anterior to the center of the parietal eye and 1.75 mm ventral to the surface of the telencephalon. Unilateral electrolytic SCN lesions (USCN-X) were performed in the same way as the bilateral lesions (23), except for the lateral lesion coordinates, which were 0.2 mm lateral and 0.8 mm anterior to the center of the parietal eye.Postsurgery Histology
The lizards were deeply anesthetized and perfused through the cardiac ventricle with Ringer solution for reptiles followed by 4% paraformaldehyde in 0.1 M phosphate buffer (pH = 7.4). Brains were removed and postfixed at +4°C overnight in the same fixative. After postfixation, brains were embedded in paraffin and cut in coronal sections on a microtome at 10 µm. Sections were stained with cresyl violet and examined to determine location and extent of the lesions (see Fig. 1).
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Experimental Protocols
Seasonal experiments. In each different season, lizards were allowed to free run in DD for 15 days, after which they were subjected to daily melatonin injections. After 25-40 days of melatonin injections, melatonin was replaced with vehicle solution and daily vehicle injections continued for 15-20 days. In some lizards, after 15-40 days of melatonin injections, the time schedule of the injections underwent a 4-h shift and the injections continued to assess reentrainment to the new schedule. Two further groups of lizards collected in spring and summer were pinealectomized (Pin-X) and subjected to daily melatonin injections in DD, respectively.
SCN experiments. Lizards collected in summer were subdivided into two groups; each lizard belonging to the first group was subjected to bilateral ablation of the SCN (SCN-X), and each lizard belonging to the second group was subjected to unilateral ablation of the SCN (USCN-X). After surgery, both SCN-X and USNC-X lizards were allowed to free run in DD for 20-30 days and were then subjected to daily melatonin injections. Some lizards were subjected to melatonin injections while free running in DD before SCN-X or USCN-X surgery, and the daily injections continued for several weeks after surgery.
Data Evaluation
The free-running period () was determined for a 10-day segment just
before melatonin injections, and further 10-day segments during
melatonin injections and/or vehicle injections were determined by means of 
2 periodogram
analysis (28). After SCN-X lesions, the locomotor activity of several
lizards became arrhythmic, as judged by visual inspection of the
records. Presence of circadian periodicities in the locomotor activity
of SCN-X lizards was tested by means of
2 periodogram analysis on a
10-day segment just before the lesion, and 10-day segments were tested
2-5 wk after lesioning. 2
periodogram analyses have been reported in the figures.
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RESULTS |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Seasonal Experiments
Circadian locomotor rhythms of nine out of ten intact lizards tested in autumn and all intact lizards tested in winter (n = 8) and spring (n = 8), respectively, never entrained to daily melatonin injections and never showed relative coordination, because the injections never affected their free-running periods (Ref. 5, Fig. 2, A-C). Pin-X lizards tested in spring (n = 5) never entrained to melatonin injections and never showed relative coordination (Fig. 3, top). Circadian locomotor rhythms of 10 out of 13 intact lizards and all (n = 5) Pin-X lizards tested in summer entrained successfully to daily melatonin injections (representative examples in Fig. 4; Fig. 3, bottom; and Fig. 5, top). Summer entrainment of locomotor rhythms to the 24-h period of the injections was confirmed by2
periodogram analysis (Figs. 4 and 3,
right, and Fig. 5,
top). In lizards entrained to
melatonin, a 4-h shift in the time schedule of injections induced
shifts of the activity onsets, which resulted, after several transient
cycles, in entrainment to the new schedule (Fig. 4). In lizards
entrained to melatonin there was a consistent phase relationship
between the time of melatonin injections and the onset of daily
activity rhythm. Melatonin injections were followed by an inactive
period 12.7 ± 1.9 h (mean ± SE, range 9.4-19 h) in
duration (Fig. 4 and Fig. 5, top).
After pinealectomy (Pin-X lizards), melatonin injections were followed
by an inactive period 16 ± 2.2 h in duration (mean ± SE, range
11.9-19.4 h) (Fig. 3, bottom).
Measurements of the preinjection periods () expressed by intact
lizards revealed that the of those individuals that subsequently
entrained to the injections were significantly shorter than those of
individuals that did not entrain to the injections [Fig.
6: n = 11, = 24.1 ± 0.12 h (mean ± SE) and
n = 28, = 25.3 ± 0.11 h (mean ± SE), respectively; P < 0.001, Mann-Whitney U test]. The
locomotor rhythms of lizards that were entrained to melatonin
injections started immediately to free run when melatonin was replaced
with vehicle solution (Fig. 4,
bottom). This demonstrates that the
entraining effects of the injections are primarily due to melatonin and
not to other aspects of the experimental manipulation.
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SCN Experiments
After bilateral SCN ablation (SCN-X), all lizards (n = 5) became behaviorally arrhythmic and remained arrhythmic during the whole period of melatonin injections. In all cases,2
periodogram analysis confirmed the abolition of circadian rhythmicity (representative example in Fig. 5, C
and D,
right). In two lizards on which
operations had been performed and which remained rhythmic and
subsequently entrained to melatonin injections (not shown), lesions
were restricted to the periventricular nuclei of the hypothalamus and
the SCN remained intact, as revealed by postexperimental histology. After unilateral SCN ablation (USCN-X), all lizards remained
behaviorally rhythmic (Figs. 7 and
8). In some USCN-X lizards free running in
constant conditions, subsequent changes in were observed before
starting with melatonin injections (Fig. 7,
top). Locomotor rhythms of six out
of eight USCN-X lizards entrained successfully to melatonin injections
(representative examples in Figs. 7 and 8). In the USCN-X lizards
that entrained to melatonin injections, there was a consistent phase
relationship between the time of injections and the onset of daily
activity rhythm. Melatonin injections were followed by an inactive
period 12.5 ± 1.4 h in duration (mean ± SE; range 8.0-16.1
h) (Figs. 7 and 8).
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DISCUSSION |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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The present results demonstrate for the first time in a vertebrate that daily injections of exogenous melatonin are capable of entraining circadian locomotor rhythmicity in only one season. Although in summer the locomotor rhythms of most intact P. sicula entrain to the 24-h period of melatonin injections, in all other seasons, the locomotor rhythms of these lizards do not entrain to the period of the injections (Figs. 2, 4, and 5, top).
Several aspects of the summer results provide clear-cut evidence of the fact that daily melatonin injections actually entrained the activity rhythm and did not merely cause masking of the underlying oscillation (Figs. 4 and 5, top): 1) steady state of entrainment to the injections was achieved only after a series of transient cycles, 2) when melatonin injections were phase shifted, the activity rhythm did not follow the phase shift instantaneously but through several transient cycles, and 3) the activity onset in the (postmelatonin injection) free-running rhythm extrapolates back to the time of activity onsets during melatonin injections. The pattern of summer entrainment of P. sicula to daily melatonin injections is similar to that observed in S. occidentalis, including the fact that in the synchronized state, the phase relationship between the time of injection and the activity rhythm of most lizards was such that the main portion of the rest time followed the time of melatonin injection (36).
In autumn (with 1 exception), winter, and spring, the failure in
entrainment of the activity rhythm of P. sicula to melatonin injections is not due to the fact
that the daily melatonin pulse produced by the injection incidentally
fell into the "dead zone" of a phase-response curve (PRC) to
melatonin. In fact, these lizards did not respond to the injections
even if, due to the remarkable length of their free-running periods,
the injections hit (in some cases several times) all phases of their
circadian cycle (Fig. 2,
A-C).
Furthermore, the only PRC to melatonin reported in a lizard
(S. occidentalis) showed that
melatonin pulses elicit phase-dependent shifts (either advances or
delays) of the activity rhythm in all phases of the circadian cycle
(i.e., no dead zone exists in the PRC) (34). On the other hand, because
our data make it clear that melatonin injections are capable of
entraining only the activity rhythm of lizards whose preinjection
free-running periods are comprised between 23.3 and 24.8 h, the
entrainment failure reported here is readily explained by the evidence
that most preinjection periods expressed by lizards in autumn, winter,
and spring clearly lie beyond that range (Fig. 6). On the contrary,
most preinjection periods expressed by lizards in summer are comprised
between 23.3 and 24.8 h, and their rhythms entrain successfully to
melatonin injections (Fig. 6). Hence the fact that in summer,
differently from all other seasons, preinjection periods are close
enough to zeitgeber period (24 h) to achieve entrainment seems to
explain the seasonal differences in the capability of melatonin to
entrain the activity rhythm of P. sicula. This suggests that melatonin may be a weak
zeitgeber in P. sicula, i.e., a
zeitgeber that is capable of entraining the rhythm only when its period
is quite close to that prevailing in free run (5). Besides, the present results confirm those of previous investigations in the same species, showing that free-running periods in autumn through winter are significantly longer than in summer and also that other features of the
circadian locomotor pattern of P. sicula vary dramatically with season (Ref. 11 and Figs.
2 and 4). They further raise the question whether the uniqueness of
summer entrainment to periodic melatonin is merely a consequence of the
incidental closeness between zeitgeber period and typical summer
free-running periods or, alternatively, whether it is an adaptive
necessity for the circadian system in summer to achieve and maintain
temporal organization of behavior during the season. If entrainment to
periodic melatonin were only due to the closeness between zeitgeber
period and summer free-running periods, we would have observed at least
some relative coordination in the activity rhythm of lizards expressing
free-running periods outside the range of entrainment (Ref. 5 and Fig.
6). In these lizards, however, relative coordination did not occur, because the injections never affected the period of their activity rhythm (Fig. 2,
A-C).
Furthermore, other results gathered in P. sicula strongly support the view that the observed
phenomenon is a summer adaptation of the circadian system. Pinealectomy
abolishes circadian rhythms of blood-borne melatonin expressed by
P. sicula in summer (9). By
lengthening , shortening , and abolishing bimodal activity,
pinealectomy in P. sicula also
abolishes the circadian locomotor pattern typical of summer (short ,
long , and bimodal activity) (14). The fact that in
P. sicula chronic administration of
exogenous melatonin (in Silastic capsules), another treatment that
virtually abolishes melatonin rhythms in the blood, induces the same
behavioral effects as pinealectomy in summer suggests that
disappearance of the summer locomotor pattern in response to
pinealectomy is due to the concomitant withdrawal of rhythmic changes
in plasma melatonin levels (10). Whether or not rhythmic changes in
plasma melatonin levels persist in autumn and winter, the fact that
pinealectomy either leaves unaffected or marginally affects the autumn
through winter locomotor pattern of P. sicula makes it clear that during these seasons melatonin rhythms are not required to maintain circadian organization in this lizard (13). Altogether, these findings demonstrate high
responsiveness of the circadian system to pineal melatonin in summer
and low or no responsiveness of the system in autumn and winter. Hence,
because only in summer (and not in other seasons) did endogenously
generated, pineal-dependent melatonin rhythms acquire a primary role in
the circadian organization of P. sicula, it is only in summer that injections of
exogenous melatonin administered periodically are expected (and were
actually found) to entrain circadian locomotor rhythms in this lizard.
Daily melatonin injections were found to entrain circadian locomotor rhythms of pinealectomized P. sicula in summer but not in spring. Besides confirming that only in summer are melatonin injections capable of entraining the activity rhythm, these data demonstrate that the pineal gland is not the primary target site of melatonin in the circadian system of P. sicula. The results are in agreement with those reported in the lizard S. occidentalis, showing that periodic melatonin entrains the activity rhythm of pinealectomized individuals (12).
Other experiments examined whether the SCN are the target sites of melatonin in the circadian system of P. sicula. To test the hypothesis above, we used a behavioral approach: we compared the behavioral response to daily melatonin injections of two different groups of summer lizards, one of which underwent bilateral ablation of the SCN and the other which underwent unilateral ablation of the SCN. SCN-X lizards became behaviorally arrhythmic, and daily melatonin injections did not restore rhythmicity in SCN-X lizards (Fig. 5). USCN-X lizards, however, remained behaviorally rhythmic, and their locomotor rhythms did entrain to the 24-h period of melatonin injections in six of eight USCN-X individuals (Figs. 7 and 8). Besides demonstrating that the presence of one SCN is sufficient to achieve entrainment of locomotor rhythms to melatonin injections, these data support the hypothesis that the SCN are the primary extrapineal target sites of melatonin in the circadian system of P. sicula. They further suggest that the SCN may mediate the central role played by endogenously generated, pineal-dependent plasma melatonin rhythms in establishing and maintaining the circadian locomotor pattern typical of summer (13). At the same time, these findings provide evidence of the fact that the target sites of melatonin within the circadian system of P. sicula are themselves circadian oscillators: 1) steady state of entrainment in USCN-X lizards to daily melatonin injections was achieved only after a series of transient cycles (Fig. 8), and 2) when melatonin injections were phase shifted, the activity rhythm of USCN-X lizards did not follow the phase shift instantaneously but rather through several transient cycles (Fig. 8). Because, moreover, summer entrainment to melatonin injections occurred in pinealectomized and USCN-X but not in SCN-X lizards, it is likely that the circadian oscillators responsive to melatonin in P. sicula are the SCN themselves. Indirect evidence suggests that the SCN play a crucial role in the circadian organization of P. sicula all year, because in all seasons 1) locomotor rhythms in DD persist after combination of pinealectomy and retinalectomy in the same individual lizard (6); 2) after removal of both the pineal gland and retinas, lizards continue to show LL-intensity-dependent changes in free-running period (i.e., they continue to obey Aschoff's rule for diurnal animals) (1, 8); and 3) electrolytic lesions to the SCN invariably abolish circadian locomotor rhythmicity (23). The SCN were also shown to be necessary for the persistence of circadian locomotor rhythmicity in another lizard, namely the desert iguana D. dorsalis (16).
There is evidence that in most vertebrates, the SCN are sites of melatonin receptors (4, 25, 27, 38). In lizards the concentration of melatonin receptors within the brain was found to be higher than in every other vertebrate species, but the localization experiments performed so far have not tested for the presence of melatonin receptors in the SCN (26, 40). In birds and mammals, plasma melatonin rhythms of pineal origin were shown to influence SCN activity (17-19). In the house sparrow (P. domesticus), for example, the SCN express circadian rhythms in 2-[125I]iodomelatonin high-affinity binding that are suppressed by pinealectomy and restored by melatonin administration (17, 18). In rats, the ability of melatonin to entrain circadian locomotor rhythms was shown to depend on the concentration of melatonin receptors in the SCN (39). The locomotor rhythms of the mink (Mustela vison), whose SCN completely lack melatonin receptors, are not entrainable by daily melatonin injections (2). If in P. sicula a similar correlation between melatonin receptor concentration in the SCN and entrainability of locomotor rhythms to melatonin were demonstrated, the seasonal changes in responsiveness of the circadian system to daily melatonin injections reported here would imply the existence of seasonal changes in melatonin receptor concentration in the SCN in this lizard, with high concentration in summer and low concentration in all other seasons.
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ACKNOWLEDGEMENTS |
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We thank Dr. Bahram Sayyaf Dezfuli and Elena Zeni for technical assistance.
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FOOTNOTES |
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This work was supported by grants of the Italian Ministero dell'Università e della Ricerca Scientifica e Tecnologica and Sigma-Tau Italia.
Address for reprint requests: A. Foà, Dipartimento di Biologia, Sezione Biologia Evolutiva, Università di Ferrara, via L. Borsari, 46, Ferrara 44100, Italy.
Received 30 July 1997; accepted in final form 2 December 1997.
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REFERENCES |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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