Seasonal influences on sleep and executive function in the migratory White-crowned Sparrow (Zonotrichia leucophrys gambelii).

BACKGROUND: We have previously shown that the White-crowned Sparrow (WCS) decreases sleep by 60% during a period of migratory restlessness relative to a non-migratory period when housed in a 12 h light: 12 h dark cycle. Despite this sleep reduction, accuracy of operant performance was not impaired, and in fact rates of responding were elevated during the migratory period, effects opposite to those routinely observed following enforced sleep deprivation. To determine whether the previously observed increases in operant responding were due to improved performance or to the effects of migration on activity level, here we assessed operant performance using a task in which optimal performance depends on the bird's ability to withhold a response for a fixed interval of time (differential-reinforcement-of-low-rate-behavior, or DRL); elevated response rates ultimately impair performance by decreasing access to food reward. To determine the influence of seasonal changes in day length on sleep and behavioral patterns, we recorded sleep and assessed operant performance across 4 distinct seasons (winter, spring, summer and fall) under a changing photoperiod. RESULTS: Sleep amount changed in response to photoperiod in winter and summer, with longest sleep duration in the winter. Sleep duration in the spring and fall migratory periods were similar to what we previously reported, and were comparable to sleep duration observed in summer. The most striking difference in sleep during the migratory periods compared to non-migratory periods was the change from discrete day-night temporal organization to an almost complete temporal fragmentation of sleep. The birds' ability to perform on the DRL task was significantly impaired during both migratory periods, but optimal performance was sustained during the two non-migratory periods. CONCLUSIONS: Birds showed dramatic changes in sleep duration across seasons, related to day length and migratory status. Migration was associated with changes in sleep amount and diurnal distribution pattern, whereas duration of sleep in the non-migratory periods was largely influenced by the light-dark cycle. Elevated response rates on the DRL task were observed during migration but not during the short sleep duration of summer, suggesting that the migratory periods may be associated with decreased inhibition/increased impulsivity. Although their daily sleep amounts and patterns may vary by season, birds are susceptible to sleep loss throughout the year, as evidenced by decreased responding rates following enforced sleep deprivation.

Sleep deprivation in pigeons and rats using motion detection.

STUDY OBJECTIVES: Forced sleep deprivation results in substantial behavioral and physiologic effects in mammals. The disk-over-water (DOW) method produces a syndrome characterized by increased energy expenditure and a robust preferentially rapid-eye-movement sleep rebound upon recovery or eventual death after several weeks of sleep deprivation. The DOW has been used successfully only in rats. This paper presents a method to enforce long-term controlled sleep deprivation across species and to compare its effects in rats and pigeons. DESIGN AND INTERVENTION: A conveyor was substituted for the DOW disk. Behavior rather than electroencephalography was used to trigger arousal stimuli, as in gentle-handling deprivation. Rats and pigeons were deprived using this apparatus, and the results were compared with each other and with published reports. MEASUREMENTS AND RESULTS: The physiologic consequences and recovery sleep in rats were like those published for DOW rats. Magnitude of sleep loss and recovery patterns in pigeons were similar to those seen in rats, but expected symptoms of the sleep deprivation syndrome were absent in pigeons. The use of a motion trigger allowed us to measure and, thus, to assess the quality and impact of the procedure. CONCLUSION: Prolonged and controlled sleep deprivation can be enforced using automated motion detection and a conveyor-over-water system. Pigeons and rats, deprived of sleep to the same extent, showed similar patterns of recovery sleep, but pigeons did not exhibit the hyperphagia, weight loss, and debilitation seen in rats.

Methylmercury and nutrition: adult effects of fetal exposure in experimental models.

Human exposure to the life-span developmental neurotoxicant, methylmercury (MeHg), is primarily via the consumption of fish or marine mammals. Fish are also excellent sources of important nutrients, including selenium and n-3 polyunsaturated fatty acids (PUFAs), such as docosahexaenoic acid (DHA). Laboratory models of developmental MeHg exposure can be employed to assess the roles of nutrients and MeHg and to identify potential mechanisms of action if the appropriate exposure measures are used. When maternal exposure is protracted, relationships between daily intake and brain mercury are consistent and orderly across species, even when large differences in blood:brain ratios exist. It is well established that low-level developmental MeHg produces sensory deficits. Recent studies also show that perseveration in reversal-learning tasks occurs after gestational exposures that produce low micromolar concentrations in the brain. A no-effect level has not been identified for this effect. These exposures do not affect the acquisition or performance of discrimination learning, set shifting (extradimensional shift), or memory. Reversal-learning deficits may be related to enhanced impact of reinforcers as measured using progressive ratio reinforcement schedules, an effect that could result in perseveration. Also reported is enhanced sensitivity to dopamine reuptake inhibitors and diminished sensitivity to pentobarbital, a GABA(A) agonist. Diets rich in PUFAs or selenium do not protect against MeHg's effects on reversal learning but, by themselves, may diminish variability in performance, enhance attention or psychomotor function and may confer some protection against age-related deficits in these areas. It is hypothesized that altered reward processing, dopamine and GABAergic neurotransmitter systems, and cortical regions associated with choice and perseveration are especially sensitive to developmental MeHg at low exposure levels. Human testing for MeHg's neurotoxicity should emphasize these behavioral domains.

Sleep deprivation in the pigeon using the Disk-Over-Water method.

A well-defined sleep deprivation (SD) syndrome has been observed in studies with rats under conditions of severe sleep loss on the Disk-Over-Water (DOW) apparatus. Observation of the sleep deprivation syndrome across taxa would assist in the elucidation of the function of sleep. In the present study, the effects of total sleep deprivation were assessed in pigeons, a biologically relevant choice given that birds are the only non-mammalian taxon known to exhibit unequivocal rapid-eye-movement (REM) sleep and non-REM (NREM) sleep. Pigeons were deprived of sleep for 24-29 days on the DOW by rotating the disk and requiring them to walk whenever sleep was initiated. Control (C) birds were also housed on the DOW and required to walk only when the deprived (D) birds were required to walk due to sleep initiation. NREM and REM sleep amounts were reduced from baseline during the deprivation for both D and C birds, although D birds obtained less NREM sleep than controls. Across the deprivation, D birds had their total sleep reduced by 54% of baseline (scored in 4 s epochs), whereas previous studies in rats on the DOW reported total sleep reduction of as much as 91% (scored in 30 s epochs). Pigeons proved to be more resistant to sleep deprivation by the DOW method and were much more difficult to deprive over the course of the experiment. Overall, the pigeons showed recovery sleep patterns similar to those seen in rats; i.e., rebound sleep during recovery was disproportionately composed of REM sleep. They did not, however, show the obvious external physical signs of the SD syndrome nor the large metabolic and thermoregulatory changes associated with the syndrome. The DOW method was thus effective in producing sleep loss in the pigeon, but was not as effective as it is in rats. The absence of the full SD syndrome is discussed in the context of limitations of the DOW apparatus and the possibility of species-specific adaptations that birds may possess to withstand or adapt to conditions of limited sleep opportunity.

Spatial and visual discrimination reversals in adult and geriatric rats exposed during gestation to methylmercury and n-3 polyunsaturated fatty acids.

Fish contain essential long chain polyunsaturated fatty acids (PUFAs), particularly docosahexaenoic acid (DHA), an omega-3 (or n-3) PUFA, but are also the main source of exposure to methylmercury (MeHg), a potent developmental neurotoxicant. Since n-3 PUFAs support neural development and function, benefits deriving from a diet rich in n-3s have been hypothesized to protect against deleterious effects of gestational MeHg exposure. To determine whether protection occurs at the behavioral level, female Long-Evans rats were exposed, in utero, to 0, 0.5, or 5ppm of Hg as MeHg via drinking water, approximating exposures of 0, 40, and 400 microgHg/kg/day and producing 0, 0.29, and 5.50ppm of total Hg in the brains of siblings at birth. They also received pre- and postnatal exposure to one of two diets, both based on the AIN-93 semipurified formulation. A "fish-oil" diet was high in, and a "coconut-oil" diet was devoid of, DHA. Diets were approximately equal in alpha-linolenic acid and n-6 PUFAs. As adults, the rats were first assessed with a spatial discrimination reversal (SDR) procedure and later with a visual (nonspatial) discrimination reversal (VDR) procedure. MeHg increased the number of errors to criterion for both SDR and VDR during the first reversal, but effects were smaller or non-existent on the original discrimination and on later reversals. No such MeHg-related deficits were seen when the rats were retested on SDR after 2 years of age. These results are consistent with previous reports and hypotheses that gestational MeHg exposure produces perseverative responding. No interactions between diet and MeHg were found, suggesting that n-3 PUFAs do not guard against these behavioral effects. Brain Hg concentrations did not differ between the diets, either. In geriatric rats, failures to respond were less common and response latencies were shorter for rats fed the fish-oil diet, suggesting that exposure to a diet rich in n-3s may lessen the impact of age-related declines in response initiation.

Gestational exposure to methylmercury and selenium: effects on a spatial discrimination reversal in adulthood.

Selenium, a nutrient, and methylmercury, a developmental neurotoxicant, are both found in fish. There are reports that selenium sometimes ameliorates methylmercury's neurotoxicity, but little is known about the durability of this protection after low-level gestational exposure. Developmental methylmercury exposure disrupts behavioral plasticity, and these effects extend well into adulthood and aging. The present experiment was designed to examine interactions between developmental low-level methylmercury and nutritionally relevant dietary selenium on discrimination reversals in adulthood. Female rats were exposed, in utero, to 0, 0.5, or 5 ppm mercury as methylmercury via drinking water, approximating mercury exposures of 0, 40, and 400 microg/kg/day. They also received both prenatal and postnatal exposure to a diet containing selenium from casein only (0.06 ppm) or 0.6 ppm selenium, creating a 2 (chronic Se)x3 (gestational MeHg) full factorial design, with six to eight rats per cell. Behavior was evaluated with a spatial discrimination procedure using two levers and sucrose reinforcers. All groups acquired the original discrimination similarly. Rats exposed to low selenium (0.06 ppm), regardless of MeHg exposure, required more sessions to complete the first reversal and made more omissions during this reversal than high selenium (0.6 ppm) animals, but the two diet groups did not differ on subsequent reversals. Rats exposed to MeHg, regardless of selenium exposure, made more errors than controls on the first and third reversals, which was away from the original discrimination. MeHg-exposed animals also had shorter choice latencies than controls during the first session of a reversal. Low selenium increased the number of omissions during a reversal, whereas high MeHg exposure produced perseverative responding (errors) on the lever that was reinforced during the original discrimination. However, there was no interaction between selenium and MeHg exposure.

Gestational exposure to methylmercury and n-3 fatty acids: effects on high- and low-rate operant behavior in adulthood.

Fish in the diet is the major source of methylmercury (MeHg) exposure, but eating fish also provides important nutrients. Many fish species contain essential long chain polyunsaturated fatty acids, especially docosahexaenoic acid (DHA), an omega-3 (or n-3) fatty acid, that is important for neural development and function. To examine interactions between MeHg and n-3 fatty acids, female Long-Evans rats were exposed, in utero, to 0, 0.5, or 5 ppm MeHg via drinking water, approximating exposures of 0, 40, and 400 mug/kg/day. They also received pre- and postnatal exposure to a diet containing either fish oil or coconut oil, creating a 2 (Diet)x3 (MeHg) full factorial design, with 6-8 rats per cell. The diets were high or marginal, respectively, in n-3 fatty acids but approximately equal in n-6 fatty acids. No exposure-related effects on developmental milestones or growth were noted. Behavior was evaluated using a series of rapidly increasing fixed ratio (FR) schedules of sucrose reinforcement; 1, 5, 25 and 75 lever presses were required for sucrose delivery, with three sessions provided at each requirement. This phase was followed by four sessions of a differential-reinforcement-of-low-rate-behavior (DRL) schedule, in which presses preceded by 10 s (or more) without a press were reinforced. Subsequently, several progressive ratio (PR) schedules that increased response requirements throughout a single session by a rate of 5%, 10%, or 20% were imposed. Rats exposed during gestation to MeHg had significantly higher response rates than controls under the large FR schedules, during the first session of DRL, and the PR 5% schedule, but neither fish oil nor coconut oil modified MeHg's effects. This finding is consistent with hypotheses that developmental MeHg exposure produced perseverative responding or altered the sensitivity of behavior to its reinforcing consequences and that certain reinforcement contingencies can unmask MeHg's effects.

Punishment in human choice: direct or competitive suppression?

This investigation compared the predictions of two models describing the integration of reinforcement and punishment effects in operant choice. Deluty's (1976) competitive-suppression model (conceptually related to two-factor punishment theories) and de Villiers' (1980) direct-suppression model (conceptually related to one-factor punishment theories) have been tested previously in nonhumans but not at the individual level in humans. Mouse clicking by college students was maintained in a two-alternative concurrent schedule of variable-interval money reinforcement. Punishment consisted of variable-interval money losses. Experiment 1 verified that money loss was an effective punisher in this context. Experiment 2 consisted of qualitative model comparisons similar to those used in previous studies involving nonhumans. Following a no-punishment baseline, punishment was superimposed upon both response alternatives. Under schedule values for which the direct-suppression model, but not the competitive-suppression model, predicted distinct shifts from baseline performance, or vice versa, 12 of 14 individual-subject functions, generated by 7 subjects, supported the direct-suppression model. When the punishment models were converted to the form of the generalized matching law, least-squares linear regression fits for a direct-suppression model were superior to those of a competitive-suppression model for 6 of 7 subjects. In Experiment 3, a more thorough quantitative test of the modified models, fits for a direct-suppression model were superior in 11 of 13 cases. These results correspond well to those of investigations conducted with nonhumans and provide the first individual-subject evidence that a direct-suppression model, evaluated both qualitatively and quantitatively, describes human punishment better than a competitive-suppression model. We discuss implications for developing better punishment models and future investigations of punishment in human choice.