Light-entrainable Oscillator Research Articles

Phase-shifting the light–dark cycle influences food-anticipatory activity in golden shiners

This study provides evidence that a circadian light-entrainable oscillator is at least partially involved in the timing of food-anticipatory activity (FAA) in a fish, the golden shiner, Notemigonus crysoleucas. Shoals of four golden shiners were fed for 11–20 days at a fixed daily time (either early night, midnight, late night, early day, midday, or late day). Most (78%) shoals developed peaks of FAA during that period of time. Food was then withheld for 7 days, and the light–dark (LD) cycle was either advanced or delayed by 6 h on the first of those days. The activity waveform of most (53–58%) shoals shifted along with the LD cycle, as indicated by significant correlation coefficients between pre- and postshift waveforms plotted relative to LD. Nonsignificant correlations were linked to low activity levels rather than to persistence of the activity peak at the old clock time. Activity shifts were gradual, taking 2–4 days, which indicates that the underlying mechanism is circadian rather than hourglass.

INTERNAL DESYNCHRONIZATION OF THE CIRCADIAN ACTIVITY AND FEEDING RHYTHM IN AN OWL MONKEY (AOTUS LEMURINUS GRISEIMEMBRA): A CASE STUDY

In the free-running circadian locomotor activity rhythm of a 7-year-old male owl monkey (Aotus lemurinus griseimembra) kept under constant light and climatic conditions (LL 0.2 lux, 25°C ± 1°C, 60 ± 5% relative humidity [RH]), a second rhythm component developed that showed strong relative coordination with the free-running activity rhythm of 24.4h and a 24h rhythm. The simultaneously recorded feeding activity rhythm strongly resembled this rhythm component. Therefore, it seems justified to infer that there was an internal desynchronization between the two behavioral rhythms or their circadian pacemakers, that is, between the light-entrainable oscillator located in the suprachiasmatic nuclei (SCN) and a food-entrainable oscillator located outside the SCN. This internal desynchronization may have been induced and/or maintained by a zeitgeber effect of the (irregular) 24h feeding schedule on the food-entrainable oscillator. The weak relative coordination shown by the activity rhythm indicates a much weaker coupling of the light-entrainable oscillator to the food-entrainable oscillator than vice versa. (Chronobiology International, 17(2), 147–153, 2000)

Forced dissociation of food- and light-entrainable circadian rhythms of rats in a skeleton photoperiod

BRINKHOF, M. W. G., S. DAAN AND J. H. STRUBBE. Forced dissociation of food- and light-entrainable circadian rhythms of rats in a skeleton photoperiod. PHYSIOL BEHAV 65(2) 225–231, 1998.—To investigate the control over drinking and feeding behavior by the light-entrainable circadian pacemaker, rats were maintained in a 12 h:12 h skeleton photoperiod for 36 days with both food and water restricted to the subjective day. During the restriction period most of the food and water intake was concentrated during the first 4 h of the subjective day. The subsequent release into ad lib conditions under the skeleton photoperiod or continuous dark showed that this increased ingestion during the subjective day persisted for up to 6–10 days. This may indicate the entrainment of a food-entrainable oscillator, which has hitherto been investigated solely in anticipatory activity. The daily activity rhythm returned to its original phase position. Thus the phase of the overt daily rhythm is eventually only determined by the phase of the light-entrainable oscillator (LEO) but can temporarily be influenced by the restriction of food and water access. This restriction apparently stimulated a food-entrainable oscillator in antiphase with the light-entrainable oscillator but failed to phase shift or entrain the light-entrainable oscillator.

The role of vasopressin in modulating circadian rhythm responses to phase shifts

Telemetered body temperature (BT), heart rate (HR), and motor activity (AC) data were collected in vasopressin-containing, Long–Evans (LE) and vasopressin-deficient, Brattleboro (DI) rats. In Experiment 1, the rats were initially exposed to a 12 h/12 h light/dark cycle under ad-libitum feeding and were then subjected to either a phase-advance or phase-delay shift of 6 h. After the phase-advance shift, neither strain adapted; however, after the phase-delay shift, both strains adapted rapidly. In Experiment 2, the animals were subjected to either a nocturnal or a diurnal restricted-feeding paradigm and were then exposed to either a phase-advance or phase-delay shift with synchronized feeding. In the nocturnal restricted-feeding paradigms, both strains rapidly adapted to both shifts. Concerning diurnal restricted- feeding, DI animals readily entrained to the presentation of food in both shifts; whereas, LE animals exhibited a confused rhythmicity. In Experiment 3, animals were subjected to a phase-advance shift, while the time of feeding was held constant. Following the shift, LE animals responded to the onset of the dark at the new time; yet, were still influenced by the presentation of food. The DI animals maintained the preshift circadian pattern and continued to be dominated by the presentation of food. These experiments indicate that circadian rhythms of LE animals are dominated by the light entrainable oscillator (LEO) in ad-libitum feeding and by both the LEO and food entrainable oscillator (FEO) in restricted-feeding. On the other hand, the circadian rhythms of DI animals are dominated by the FEO unless food is provided ad-libitum. The demonstrated role of vasopressin in synchronizing circadian rhythms to the LEO may be of significance in understanding human circadian rhythm disturbances, such as jet lag.

Time-course studies on plasma glucose, insulin, and cortisol in sea bass ( Dicentrarchus labrax) held under different photoperiodic regimes

CERDá-REVERTER, J. M., S. ZANUY, M. CARRILLO AND J. A. MADRID. Time course studies on plasma glucose, insulin, and cortisol in sea bass (Dicentrarchus labrax) held under different photoperiodic regimes. PHYSIOL BEHAV 64(3) 245–250, 1998.—Daily variations of insulin, cortisol, and glucose are studied in animals adapted to two different photoperiodic regimes, with the intervals between feeding times and photoperiodic events kept constant. Data support the existence of a daily rhythm of plasma glucose which seems to be photoperiodic. In contrast, the daily patterns of insulin in sea bass seem to be mainly influenced by feeding time; however, an effect of photoperiod can not be excluded. When the digestive tract is absent of food, insulin levels are generally minimal at feeding times and maximal during the inter-meals periods, suggesting the central control of insulin secretion during short-term food deprivation. Contrarily, the nadir values of plasma cortisol were reached at midday during the inter-meal period and peak plasma levels were evident at both light onset and offset. Disruption between metabolite and hormone patterns suggest that they are under different controls. Such results could be explained under the existence of a multioscillator system, including a food entrainable oscillator in addition to the master light entrainable oscillator.

Entrainment of Aged, Dysrhythmic Rats to a Restricted Feeding Schedule

Aged rats often display abnormal circadian activity rhythms; the rhythm amplitude is low and entrainment to light-dark cycles is irregular. The activity rhythm of young rats can be entrained by both light and nonphotic cues, specifically food availability. In young rats, entrainment to restricted feeding cycles does not depend on intact suprachiasmatic nuclei, the presumed anatomical location of the light-entrainable oscillator. In this study, aged rats that displayed disrupted entrainment to light were assessed for their ability to entrain to restricted feeding schedules. Aged rats, young controls, and young suprachiasmatic nuclei-lesioned (SCN) rats were placed on a food restriction schedule (FR) for 14 days. Food was available for 2 h during the light phase of a 12-h light-dark cycle. Despite the absence of entrainment to light/dark cycles, both SCN-lesioned and aged groups showed entrainment to FR, with clear bouts of anticipatory activity during a period of complete food deprivation following 2 weeks of FR. The results suggest that the dysrhythmia of aged rats is a result of natural deterioration of a central circadian light-entrainable pacemaker, but that a secondary oscillator entrainable to food cycles is spared.

Coupling between light- and food-entrainable circadian oscillators in pigeons

Two experiments were conducted with a restricted feeding schedule to determine whether pigeons have a separate food-entrainable oscillator (FEO) and to assess the coupling strength between the FEO and the light-entrainable oscillator (LEO). In the baseline condition, the body temperature ( T b) and O 2 consumption of two pigeons increased prior to light onset (LD 12:12 cycle) and food presentation (at the ninth hour of the light phase). In one experiment, when the LD cycle was phase delayed or advanced by 4 h while feeding time remained unchanged, the T b and O 2 rises prior to light-onset showed the expected delaying or advancing transients, but the rises prior to feeding also delayed or advanced for several days before returning to their proper phase position. In the second experiment, food was presented at 23.5-h intervals for 10 days while the LD cycle continued with a 24-h period. Entrainment to the LD cycle was unaffected, and T b and O 2 consumption continued to rise prior to the changing feeding time, but with a reduced lead time. When the feeding time was subsequently delayed by 5 h, T b and O 2 consumption with regard to the LD cycle were unaffected, but delaying transients occurred until both measures reentrained to the new feeding time. The results provide support for the existence of a separate FEO in pigeons and indicate asymmetrical coupling between the LEO and FEO, with the former having a stronger effect on the latter.

Light-dark and food restriction cycles in sea bass: Effect of conflicting zeitgebers on demand-feeding rhythms

Sea bass, a fish species characterized by its dualistic feeding pattern, was investigated to study the synchronizing effect of light and food on the demand-feeding rhythm. Nocturnal and diurnal sea bass, both in groups and individually, were exposed to restricted-feeding (RF) and light-dark (LD) cycles of different periods. The phase relationship between both zeitgebers was also studied. The results show that food-demand rhythms synchronize to periodic food availability under constant light conditions (DD) and that there is a partial coupling between food-entrained and light-entrained activity under conflicting zeitgebers (LD 13:13 h and RF 4:20 h), suggesting the existence of a feeding entrainable oscillator (FEO) in addition to the master light entrainable oscillator (LEO). In some cases, food availability restricted to the light or dark phase contrary to that of the previous feeding phase changed a diurnal feeding pattern into nocturnal and viceversa, suggesting that food can be one of the switching factors that decides whether the circadian system of sea bass is nocturnal or diurnal. However, the fact that the feeding pattern of some fish was unrelated with the phase in which food was available suggests that other internal and/or external factors could be involved in the temporal flexibility of sea bass.

Ontogeny of the rabbit's circadian rhythms without an external zeitgeber

We have monitored parturition and different behavioral rhythms of does, the activity of suckling pups and behavioral rhythms of rabbits after weaning until adulthood. All animals were living in continuous light conditions (LL). As a consequence of the free-run of the does parturition, which takes place during the resting period of the animal, occurred at almost any time of the day. The once/day nursing was advanced during the first 7–10 days until it was in synchrony with the time of main activity. The pups significantly anticipated nursing by day 5: the 60 min bin prior to nursing exceeded the 24-h mean by 63 ± 30%. The anticipatory activity (AA) was entrained by an artificial nursing schedule of T = 24 h, the 60 min bin prior to nursing exceeding the 24-h mean by 123 ± 50%. Since AA persisted during a 48 h fast, its phase is controlled endogenously. At weaning behavioral rhythms of rabbits free-ran with a main tau <24 h (average 23:35 ± 17′), period length extending with increasing age. 7 10 animals had an additional component >24 h (average: 24:24 ± 16′) which became increasingly dominant, the components <24 h fading out within 30 days after weaning. Between days 340–350 a stable period length of 24:35 ± 8′ and a consolidation of the circadian rhythms was attained. These results confirm that during the first days of the rabbit's life the circadian system is controlled by a feeding entrainable oscillator, the light entrainable oscillators taking over control later.

Two meals promote entrainment of rat food-anticipatory ant rest-activity rhythms

Ten female rats were fed early and late in the dark period of a 12-12 h light-dark cycle and then were fed at the same times in constant darkness. In both conditions rats were active prior to mealtimes and manifested no free-running components of activity. When the rats were placed in constant darkness and either were fed early and late in the inactive period, or had free access to food, six of the rats had rest-activity rhythms different from 24.0 h. Though a masking explanation could not be ruled out, two meals during the active period apparently entrained the rest-activity rhythms of these rats. The light-entrainable oscillator appears to integrate information from cycles of both illumination and food availability. Multiple sources of temporal information may promote more stable entrainment of the rest-activity rhythm than the light-dark cycle alone, especially in a burrow dwelling organism, like the rat, that can be exposed to inconsistent light-dark transitions.

Circadian food-anticipatory activity: Formal models and physiological mechanisms

Rats and other species exhibit food-anticipatory activity (FAA) to daily mealtime under circadian (24 h) food access schedules. A critical review of several explanatory models indicates that hourglass clocks and associative learning processes are inadequate to explain many properties of FAA in intact and suprachiasmatic nuclei ablated rodents. A computational learning model, involving circadian clock consultation and phase memory, accounts for some but not all of these properties. An entrainment model, invoking separate, compound food- and light-entrainable oscillators, provides a more complete account of FAA. However, FAA may be simulated best by a model that combines oscillator entrainment with clock consulation and memory for circadian phase. Species as diverse as bees, birds, and mammals appear to share many features of FAA in common; differences may be explained in terms of oscillator organization and the ability to represent multiple circadian phases memorially. Physiological mechanisms of FAA are largely unknown; strategies for localization of entrainment pathways and oscillators, and a modest data base, are reviewed.

Effects of Daily Schedules of Forced Activity on Free-Running Rhythms in the Rat

Circadian rhythms of hamsters can be phase-shifted or entrained by single or daily sessions of induced wheel running. In contrast, observations of rats under restricted-feeding schedules suggest that their free-running rhythms are not readily entrainable by a daily bout of intense activity. A formal test of this idea was made by subjecting rats to daily 2-hr or 3-hr sessions of forced treadmill activity. None of 18 rats entrained to a daily treadmill schedule when tested in constant dim light, but 1 of 16 did entrain when tested after blinding, when the period of its free-running activity rhythm was very close to the period of the treadmill schedule and when the onset of its daily active phase overlapped with the treadmill sessions. These conditions were recreated in a final group of eight rats; the rats were trained in a light-dark cycle, blinded, and subjected to a treadmill schedule with a period of 23.91 hr that was initiated at the onset of the rats' active phase on day 1. Six of these rats entrained. The mechanism for entrainment by activity schedules clearly exists in rats, but the conditions under which this occurs are highly constrained, suggesting that activity is a very weak zeitgeber in this species. It is argued that the evolution of functionally separable food- and light-entrainable oscillators in the rat demands a very low sensitivity to feedback effects of activity.

Characteristics of Food-Entrained Orcadian Rhythms in Rats During Long-Term Exposure to Constant Light

Rats possess a system of circadian oscillators that permit entrainment of circadian activity rhythms independently to 24 hr cycles of light-dark and food access. The nature of interactions between food- and light-entrainable oscillators was examined by observing the generation and persistence of food-entrained circadian rhythms in rats whose light-entrainable rhythms were eliminated by long-term exposure to constant light. Most of these rats showed a delayed generation of food-entrained rhythms and only one of eight animals showed persistence of food associated rhythms during a 4-day food deprivation test. Rats whose light-entrainable rhythms are eliminated by suprachiasmatic nuclei ablation show, in contrast, normal generation and persistence of food-entrained rhythms. The results suggested a disruptive influence of constant light on non-photic entrainment, possibly due to coupling forces between damped light-entrainable oscillators and the food-entrainable oscillators.