Photoinducible Phase Research Articles

Entrainment of circadian system under variable photocycles (T‐photocycles) alters the critical daylength for photoperiodic induction in blackheaded buntings

AbstractThe present study was designed to investigate the photoperiodic responses of blackheaded buntings to various T‐photocycles [T =the period length of light:dark (LD) cycle]. Two series of experiments were performed. In series I, groups of buntings (n =8‐12) were exposed to LD cycles of 22 to 26 hr with photoperiods of 6, 10, or 11 hr (T22 =6L:16D, 10L:12D, 11L:11D; T24 =6L:18D, 11L:13D; T26 =6L:20D, 11L:15D). Among these groups, birds subjected to 11L:11D showed heavy deposition of fat, weight gain, and testicular recrudescence, a response that is characteristic of long day (≥ 12 hr photoperiod per day) photostimulation, indicating that a T‐photocycle of less than 24 hr (T =22 hr) was photoinductive in buntings when presented with a photophase long enough to interact with the photoinducible phase (ϕi), located in the middle of the photocycle. Experiments in series II included an interrupted‐night lighting protocol with a main photophase of 6 hr and 1‐hr light break in photocycles of T =22 hr, T =24 hr, and T =26 hr. The results revealed that a 1‐hr light pulse was inductive when it was introduced in the middle of the photocycles, and, thus, was coincident with the ϕi. It is suggested that the critical daylength for photoperiodic induction in buntings is altered as a result of entrainment to various T‐photocycles. © 1995 Wiley‐Liss, Inc.

A pacemaker-slave model for the photoperiodic clock in the vetch aphid, Megoura viciae

Recent investigations into the photoperiodic clock of Megoura viciae indicated that night-length measurement in this aphid is accomplished by a circadian-based oscillator mechanism, despite its typical “hourglass” responses in Nanda-Hamner and Bünsow experiments. To reconcile these apparently contradicting observations, it is suggested here that although long-night determination is executed in a repetitive manner, this is not true for short-night determination. To test this hypothesis, the previously developed “coupled oscillator model” has been modified such that once a scotophase has exceeded the critical night length (as in the Nanda-Hamner experiments) it will always be determined as “long”, no matter whether a subsequent “photo-inducible phase” coincides with darkness or with light. In this respect the modified model differs from all known circadian-clock models. Model-generated responses are compared with a variety of experimental results previously observed with Megoura and the validity of the model as a description of the photoperiodic clock-counter mechanism in Megoura is discussed.

Effects of different lighting regimes on daily hormonal and behavioural rhythms in the pregnant ewe and sheep fetus.

1. We have studied the effect of altering the time of darkness during a 12 h photoperiod on the diurnal rhythms of maternal and fetal plasma melatonin and prolactin concentrations and fetal breathing movements (FBMs) in the late pregnant sheep. 2. Four ewes were exposed to a 'normal' 12 h light-12 h dark regime with lights off at 19.00 h. Eight ewes were exposed to an 'altered' 12 h light-12 h dark regime with lights off at 11.00 h. FBMs were recorded continuously and 2 hourly maternal and fetal blood samples taken during 24 h experiments between 120 and 138 days gestation. 3. Plasma melatonin concentrations were higher during the hours of darkness in the ewes and fetuses in both the normal and altered groups; i.e. altering the time of darkness was associated with a shift in the timing of the daily increase in melatonin concentrations in the mother and fetus. 4. In the fetuses, the mean 24 h plasma prolactin concentration was higher in the altered lighting group (28.8 +/- 6.1 micrograms/l) compared to the normal lighting group (13.0 +/- 3.9 micrograms/l). There was no difference, however, between groups in the daily variation of fetal plasma prolactin concentrations, which were higher at 17.00-01.00 h than at 05.00-19.00 h. Thus, altering the time of darkness did not change the timing of the daily plasma prolactin rhythm in the fetus. 5. Under the normal lighting regime maternal plasma prolactin concentrations were higher at 17.00-19.00 h (i.e. from 2 h before lights off) than at 09.00-11.00 h. In contrast, under altered lighting, plasma prolactin concentrations were higher at 01.00-07.00 h (i.e. 2-8 h after lights on) than at 09.00 h. 6. In the normal lighting group the incidence (min/h) of FBMs were highest at 16.00-21.00 h and reached a minimum at 05.00-06.00 h. In contrast, in the altered lighting group the incidence of FBMs was lowest at 19.00-20.00 h and reached a maximum at 11.00-12.00 h. 7. The results suggest that the light-dark cycle influences the diurnal modulation of FBMs, but not the daily variation of fetal plasma prolactin concentrations. The role of plasma melatonin concentrations, and evidence for a photo-inducible phase of increased prolactin secretion in the fetus, is discussed.

A circadian clock measures photoperiodic time in the male lizard Anolis carolinensis

Photoperiod plays an important role in controlling the annual reproductive cycle of the male lizard Anolis carolinensis. The nature of photoperiodic time measurement in Anolis was investigated by exposing anoles to 3 different kinds of lighting paradigms (resonance, T cycles, and night breaks) to determine if photoperiodic time measurement involves the circadian system. Both the reproductive response and the patterns of entrainment of the activity rhythm were assessed. The results show that the circadian system is involved in photoperiodic time measurement in this species and that a discrete photoinducible phase resides in the latter half of the animals' subjective night. Significantly, the ability of the circadian system to execute photoperiodic time measurement is crucially dependent on the length of the photoperiod. Resonance, T cycle and night break cycles utilizing a photoperiod 10–11 h in duration reveal circadian involvement whereas these same cycles utilizing 6 or 8 h photoperiods do not.

Insect photoperiodism: the linden bug,Pyrrhocoris apterus, a species that measures daylength rather than nightlength

Independent variation of the dark and light components of the daily photocycle has shown that the linden bug,Pyrrhocoris apterus, unlike other species, ‘measures’ daylength rather than nightlength. Greatly extended dark periods coupled with a short photophase (a Nanda-Hamner protocol) shows peaks and troughs of diapause at about 16-h intervals, an extremely short period for a circadian clock. If circadian oscillations are involved in photoperiodic time measurement in this species, a photoinducible phase might lie in the early rather than the late subjective night.

Rapid photoperiodic responses in Japanese quail: is daylength measurement based upon a circadian system?

Experimental photoperiods, presented either once only or repeatedly, were used to assess the oscillatory and hourglass properties of the photoperiodic clock in Japanese quail. Gonadectomized quail on 8-hr daylengths respond to a single skeleton photoperiod consisting of two 8-hr light pulses separated by 2 hr of darkness (i.e., LDLD 8:2:8:6) with a marked increase in secretion rate of luteinizing hormone (LH). This response suggests that the second light pulse interacts with a "photoinducible phase" (phi i) lying some 10-16 hr from "dawn" (start of the first light pulse). If, however, groups of quail maintained on 8-hr daylengths are transferred to continuous darkness (DD), and the position of the phi i is sought by a single 8-hr light pulse applied at various times on the first or third day of DD, then an increase in circulating LH is, at best, barely detectable. It would appear that a strongly responsive phi i does not recur rhythmically in DD. Instead, the light pulse apparently acts primarily as a "dawn" signal that triggers a single cycle of photoinducibility, since a second 8-hr light pulse, placed to begin 2 hr after the end of the first, induces a large increase in plasma LH. Similar results are obtained if any single 8-hr light pulse presented to animals held in darkness is preceded, 10 hr earlier, by a short "dawn" light signal. Such dawn signals can be effective when very short; a pulse of only 30 sec can cause a subsequent phi i. The dawn pulse is effective at any circadian phase and leads to a single cycle in photoinducibility. In contrast, a much longer light pulse (perhaps not less than 4 hr) is needed to interact with phi i if significant gonadotropin secretion is to be stimulated. In confirmation of the findings described above, we found that Nanda-Hammer lighting schedules have remarkably little effect in stimulating gonadotropin secretion in gonadectomized quail. There is, for example, a very marked difference between the effectiveness of "resonating" schedules such as LD 6:6, which stimulates a high LH secretion rate since each "inductive" light pulse is preceded by an appropriate "dawn" signal, and a theoretically effective schedule such as LD 6:30, which induces a very small response by comparison. Such schedules (even theoretically noninductive ones) can, however, be made very highly inductive if alternate light pulses are preceded by an appropriately positioned 15-min light pulse to act as "dawn."

Circadian control of photoperiodic responses in a female migratory bunting ( Emberiza bruniceps)

The photoperiodic response of female redheaded bunting ( Emberiza bruniceps) was investigated in photosensitive and photorefractory birds exposed to resonance lighting cycles. Ovarian growth was stimulated in resonance cycles where light was present during the predicted photoinducible phase. Photorefractoriness was dissipated by resonance cycles in which light did not fall at times corresponding to the photoinducible phase. It is concluded that photosensitive and photorefractory female redheaded bunting monitor the photoperiodic time by means of a circadian rhythm.

Daily rhythm of cortisol, and evidence for a photo-inducible phase for prolactin secretion in nonpregnant mares housed under non-interrupted and skeleton photoperiods.

Studies were conducted in anestrous mares to characterize daily rhythms of cortisol in non-interrupted [ambient and 16 h light (L): 8 h dark (D)] and skeleton (10L:4D:2L:8D, 10L:6D:2L:6D and 10L:8D:2L:4D) photoperiods, and to determine if there exists a photosensitive phase for the secretion of prolactin. Neither peak or nadir concentrations of cortisol, nor the time of peak or nadir concentrations differed among photoperiod treatments. Highest concentrations (66 +/- 4.4 ng/ml, mean +/- SE) occurred between 0700 and 0900, whereas lowest concentrations (31 +/- 3.6 ng/ml) were found from 1900 to 2300. Mean daily concentrations of serum prolactin were significantly higher in mares housed under the 16L:8D and the 10L:8D:2L:4D photoperiods as compared with the remaining photoperiod treatments, and were lowest in the ambient photoperiod treatment. The mean daily concentration of prolactin in February among photoperiod treatments was inversely related to the number of days (from December 1) to first seasonal ovulation (r = -.92, P = .027). The results were interpreted to: 1) suggest that mares in the 10L:8D:2L:4D skeleton photoperiod do not phase-shift to interpret the 2-h light pulse as the beginning of their subjective day; and 2) provide further evidence that the photo-inducible phase for both prolactin secretion and the stimulation of seasonal reproductive activity occurs 8 to 10 h following the onset of the dark period (scotophase).

Many circadian oscillators regulate developmental and behavioural events in the flesh-fly, Sarcophaga argyrostoma.

In the flesh-fly, Sarcophaga argyrostoma, the initiation of larval wandering, pupal eclosion, and the induction of pupal diapause by seasonal changes in night length, are all regulated by circadian oscillators. They differ, however, in several respects. The rhythm of larval wandering shows a free-running period (tau) of about 20 hr and a steady-state phase-relationship to the light cycle (psi) in which maximum activity occurs at dusk or in the night; that for pupal eclosion shows tau close to 24 hr and psi close to dawn; and that for diapause induction tau longer than 24 hr and a photoinducible phase (phi i) late in the subjective night. The three oscillators are, therefore, considered to be functionally separate. In addition, adult locomotor activity, the deposition of cuticular growth layers on thoracic apodemes, and the duration of larval wandering, are possibly regulated by further, distinct, oscillators. The circadian system in S. argyrostoma, therefore, contains at least three, and probably as many as six, known circadian pacemakers.

Effects of interrupted photoperiods on the induction of ovulation in anestrous mares.

The ability of interrupted photoperiods to induce early estrus and ovulation was examined. Horse mares were exposed to long (16 h light) or short (10 h light), noninterrupted photoperiods, ambient light, or various interrupted photoperiod treatments from December 1 to April 15 (135 d). Follicular development was assessed by rectal palpation and estrous behavior was determined by teasing with a stallion. Serum concentrations of progesterone were used as an indicator of corpus luteum function. Differences among the light treatment groups were compared for the following behavioral and ovarian characteristics: days to first detectable 3-cm follicle, days to first estrous behavior, days to first ovulation, the number of mares ovulating within the treatment period, and the number of ovulations within the treatment period per mare. Compared with the ambient and 10L:14D (L = h of light and D = h of darkness) photoperiod treatments, ovulation was advanced to the greatest extent by a photoperiod of 16L:8D and the interrupted photoperiod 10L:8D:2L:4D. These two stimulatory photoperiod treatments were characterized by the presence of light 8 to 10 h after dusk. Therefore, the present data are consistent with an external coincidence model for the induction of seasonal breeding in horses, with the photoinducible phase occurring within the period 8 to 10 h after dusk.

Circadian Rhythmicity and the Initiation of Reproductive Functions in Female Passerines

Photosensitive female rose finches and yellow-throated sparrows were held under six photoperiodic regimens, consisting of a 6-h light period combined with dark periods of various durations. Ovarian growth (as well as oviducal growth in yellowthroated sparrows) was stimulated under cycles of 12 (6L:6D), 36 (6L:30D), and 60 (6L:54D) h, but not under cycles of 24 (6L: 18D), 48 (6L:42D), and 72 (6L:66D) h. These results are consistent with the Bunning hypothesis according to which a photoperiodic response occurs as the result of the coincidence of light with the photoinducible (photosensitive) phase of an endogenous circadian rhythm. The results indicate that circadian rhythmicity is involved during the initiation of the female reproductive system, as is true of many males, in photoperiodic birds.

Photoperiodic time measurement in seasonal reproduction of the weaver bird ( Ploceus philippinus)

Use of a circadian clock in photoperiodic time measurement is demonstrated in the tropical photoperiodic weaver bird with the help of resonance, ahemeral, and asymmetrical skeleton photoperiods. Different asymmetrical skeleton photoperiods and seasonal scotophase scans indicate (1) that light entrains endogenous circadian rhythms (ECR) of photosensitivity and the position of the photoinducible phase shifts according to the length of the basic photoperiod, (2) a seasonal variation in response to asymmetrical skeleton photoperiods, and (3) dissociation in the two gonadotrophins LH and FSH and a possibility of two distinct ECRs of photosensitivity for LH and FSH. Annual phasing of the ECRs of photosensitivity of the two gonadotrophins and/or interaction of hormones might be involved in the seasonal reproduction and photosensitivity of this bird.

Evidence of a photoinducible phase for the release of luteinizing hormone in the domestic hen.

Hens raised on a schedule of 8 h light: 16 h darkness (8L : 16D) were exposed to changes in photoperiod at 17 or 18 weeks of age. These involved exposure to either an abrupt increase in photoperiod to 16 h per day or to skeleton photoperiods comprising a main period of 7·75 or 4 h light together with a pulse of 15 min or 4 h light provided at different times during the period of darkness. An increase in photoperiod to 16 h per day stimulated a two- to threefold increase in the plasma concentration of LH within 1–3 days. Interruption of a 7·75L : 16D schedule by 15 min light between 13·75 and 19·75 h after the beginning of the main photoperiod stimulated LH secretion in the immature and adult hen and a higher rate of lay than that of the 8L : 16D control group. There was a significant (P < 0·01) correlation between the concentration of LH in the plasma and the rate of lay. The photostimulated rise in the plasma concentration of LH in the immature hen was not associated with any increase in the responsiveness of the pituitary gland to LH releasing hormone. Of the treatments in which a 15-min pulse of light was provided, the schedules of 7·75L : 10D : 0·25L : 6D and 7·75L : 12D : 0·25L : 4D, which were most effective in stimulating LH release, appeared to be interpreted as 0·25L : 6D : 7·75L : 10D and 0·25L : 4D : 7·75L : 12D respectively. In hens given a 7·75-h main photoperiod, in which phase-reversal did not occur, 15 min light was most stimulatory when given 14–16 h after the begining of the main photoperiod, although not to the same extent as an increase in photoperiod to 16 h per day. In hens for which an 8-h complete photoperiod was changed to a 4-h main photoperiod, together with a further 4-h pulse of light provided at different times during the period of darkness, the period of maximum sensitivity to light occurred 11 h after the onset of the main photoperiod and at this time light stimulated LH release to the same extent as an increase in complete photoperiod from 8 to 16 h per day. Results of this study suggest that the period of maximum photosensitivity shifts its phase after a change in the form of photoperiod and is primarily entrained to dusk.

Formal properties of the circadian system underlying photoperiodic time-measurement in Japanese quail

The photosensitive phase for the photoperiodic response of Japanese quail was delineated with 3 h main photoperiods and 0.25 h night breaks in cycles (T) of 24 and 27 h. UnderT24 there was one peak of induction of testicular growth and luteinizing hormone release, while underT27 there were two, the first of which had a phase angle which was about 1.5 h more positive than that of the peak inT24. In contrast, the phase angle of locomotor activity underT27 was 3–4 h more positive than underT24. During entrainment to 1 h photoperiods in cycles between 19.1 and 25.7 h in length the rate of testicular growth (k) remained close to zero even though the subjective night of the activity rhythm was illuminated in some treatments. The ratek also remained close to zero when quail were exposed to 3 h photoperiods in cycles between 21 and 36 h in length, and underT30 the critical daylength for photoperiodic induction was only 1.5 h shorter than that underT24. The results suggest that asT is altered the changes in the phase angle of the photoinducible phase are smaller than those of the rhythm of locomotor activity, indicating the involvement of oscillators with different entrainment properties. This hypothesis is neither supported nor excluded by consideration of the internal coincidence model.

Photoinducible phase for gonadotropin secretion entrained to dawn in Japanese quail.

Abstract In previous studies ( Wada, 1979 , Gen, Comp. Endocrinol. 39 , 141–149), testicular growth and LH secretion were induced when 0.5-hr (0.5L) light pulses were given to quail kept under 8L:16D during dark periods 13–15 hr after dawn. These results strongly suggested the existence of a photoinducible phase for gonadotropin secretion. To examine whether this photoinducible phase exists in different photoperiods and whether the phase is entrained to dawn or dusk, 0.5L pulses were delivered during the dark phases of 4L:20D and 11L:13D, respectively. In both cases, LH and FSH secretion, and eventually testicular growth, were induced when 0.5L pulses were given 13 hr after dawn. In 11L:13D groups, 0.5L pulses given 19 hr after dawn also induced LH increase after 5 and 10 days of treatment along with testicular growth. The response at 19 hr could be due to phase shifting and entrainment to the 0.5L pulse, which results in coincidence of the photoinducible phase with the main photoperiod of the following day and in induction of gonadotropin release. LH and FSH release is apparently induced when light impinges on the circadian photoinducible phase entrained to daybreak.

Influence of photoperiod on the time of parturition in the rat. II. Demonstration of a photoinducible phase and determination of some of its characteristics.

Parturition time has been chosen to investigate whether a photoinducible phase exists during the light-dark cycle in the rat. A 1-hr light stimulation was given during the dark phase at various times after the beginning of the principal photoperiod or conventional dawn. The rats kept under 8 hrs of light and 16 hrs of darkness from mating (day 1 of pregnancy) gave birth to most of their pups on the afternoon of day 22 of pregnancy when the light pulse was applied 9 to 18 hrs or 22 to 23 hrs after dawn. Parturition was delayed till day 23 when the light pulse was given 18 to 22 hrs after dawn. In the same manner, under 16 hrs of light and 8 of darkness, most of the parturitions occurred on day 23 of pregnancy when a light pulse was given 22 hrs after dawn; they extended over two preferential periods--one on day 22 (about 50 p. 100) and the other on day 23 when the light pulse was given 16 to 17 hrs or 18 to 19 hrs after dawn. Thus, the stimulation of the photoinducible phase, found at the end of the dark period, resulted in retarded parturition. That delay was also observed when the light pulse was only given during the final days of pregnancy. Most parturitions occurred on day 22 of pregnancy under a short photoperiod to which 5 hrs of light were added during the dark phase at a time not coinciding with the photoinducible phase. This suggested that the effect of the principal light regime and the stimulation of the photoinducible phase could be dissociated.

Photoperiodic control of LH secretion in Japanese quail with special reference to the photoinducible phase

Repetitive blood sampling from Japanese quail showed that plasma LH concentration rose during the first dark period after the birds were transferred from 8L:16D to 16L:8D. In the second light period of long days, LH concentration decreased slightly (not significant) and maintained this lower level until the second dark period of long days. During the second dark period LH again increased. This suggests that at the first stage of LH release by long photoperiod, photoinduction can occur at least during 8 to 16 hr after lights are turned on. To test the hypothesis that LH secretion induced by long days is dependent on the photoinducible phase, 0.5-hr light pulses (0.5L) were given to quail kept under 8L:16D during the dark periods. Activity was also recorded for each bird. After 10 days of treatment, testicular growth was induced when 0.5L pulses were given at 13 or 19 hr after dawn. Testicular growth induced by 0.5L pulses given at 19 hr after dawn was less than that in birds given light 13 hr after dawn and had greater individual variation compared with other groups. The activity records of these birds revealed that some remained entrained to the primary light pulse (8 hr) while others phase shifted to the short pulse (0.5 hr). The latter were, in effect, then exposed to a 13-hr photoperiod while the former were exposed to 8L:11D: 0.5L:4.5D. LH increase by 0.5L given during the dark period was detected after 2 days of treatment when the pulses were delivered at 15 hr after dawn. These results suggest that LH release is induced when light impinges on the circadian photosensitive phase which is set by external lighting schedules.

External coincidence and the photoinducible phase in theSarcophaga photoperiodic clock

1. Data from single light pulse resetting experiments on the circadian rhythm of pupal eclosion inSarcophaga argyrostoma were used to design and predict the outcome of one- and two-pulse cycles in terms of the induction of pupal diapause. Experiments were interpreted in terms of the “External Coincidence” model of Pittendrigh (1966). 2. Two-pulse asymmetrical “skeleton” photoperiods (night-interruption experiments), in which a short supplementary pulse scans the “night” of a diapause-inductive cycle, show two points (A and B) of short-night effect (the non-diapause or “summer” pathway). The External Coincidence model suggests that the photoinducible phase (φi) lies at point B. 3. Single short pulses of light (1 h) were used in cycles of different length (so-called T-experiments) in such a way that the light pulses fell on particular circadian phases in each cycle. “Short-night” or non-diapause effects were only produced when the light pulse fell, in each cycle, on that phase (Circadian time, Ct, 21.5) equivalent to point B. 4. In T-experiments comprising l h pulses of light in a cycle of LD 1∶20.5 (T 21.5), with the first pulse in the train starting at different circadian phases, the incidence of diapause was shown to be a function of the number of transient cycles before the circadian pacemaker achieved steady-state entrainment to the light cycle. 5. In two-pulse asymmetric “skeletons” in which the scanning pulse was arranged to fall on point A, it was shown that the diapause-averting effects of the scanning pulse could be “reversed” by a terminal dark period greater than the critical night length. In asymmetrical skeletons in which the pulse fell on point B, however, the diapause-averting effects were irreversible. These experiments demonstrate that the photoinducible phase lies late in the subjective night at a circadian phase (Ct 21.5) marked by point B in night interruption experiments. 6. Although the results do not exclude the possibility of an “Internal Coincidence” type of photoperiodic clock (Pittendrigh, 1972) they remain consistent with the External Coincidence model as adopted in earlier papers forS. argyrostoma. The results also underscore the essential similarities between the photoperiodic clocks inSarcophaga and the aphidMegoura viciae (Lees, 1973).

Night length measurements by the circadian clock controlling diapause induction in the mosquito Aedes atropalpus

Night interruption experiments were used to investigate the behavior of the clock controlling diapause induction in the mosquito, Aedes atropalpus. The data from these experiments indicated that the clock included a circadian oscillator which was phase set at dusk. Following this event the oscillator proceeded to drive a nightly rhythm of sensitivity to light. This rhythm included a photoinducible phase where light interruption inhibited diapause. The photoinducible phase was fixed, occurring 7 to 9 hr after dusk in all photoperiod regimens tested. The photoinducible phase was followed by a refractory phase, which continued until dawn. During the refractory period light did not inhibit diapause. These observations indicated that the circadian clock behaved like an interval timer which was set at dusk. The rhythm of sensitivity to light, an inherited time scale, limited the induction of diapause to seasonal periods when nights were longer than 9 hr. As a result, diapause was induced only when the daylength dropped below the critical photoperiod of L15:D9 (hours of light:hours of dark). A ‘T’ experimental design was used to confirm the importance of the length of the night in clock controlled induction of diapause in this mosquito.

Light control of prolactin secretion in sheep. Evidence for a photoinducible phase during a diurnal rhythm

Light control of prolactin secretion in sheep. Evidence for a photoinducible phase during a diurnal rhythm