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

Abstract

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.

Figure 1

This double plotted actogram shows activity for a representative bird over the course of approximately 30 months, including 2005 when the sleep data for this paper were collected. Vertical yellow lines indicate seasonal changes in daylight. Seasons from which birds were selected for sleep analyses are highlighted (winter (blue) n = 4, spring (green) n = 5, summer (red) n = 4, fall (brown) n = 3). Photoperiods for the winter, spring, summer, and fall seasons were, respectively, 9.5:14.5 LD, 14.75:9.25 LD, 21.5:2.5 LD, and 13.75:10.25 to 16.0:8.0 LD.

Figure 2

Time course of each vigilance state, wake (red), sleep (purple) and drowsiness (purple), in each of the four seasons. Values plotted as mean number of minutes (± SEM,) of each state in 1-hour intervals. Time 0 represents lights on. Note that the fall birds were not scored on the same day and so each bar indicates the dark period for one of the three birds.

Figure 3

States of vigilance as a function of light and dark. Figure 3A. Box-and-whisker plots comparing percentage of time spent in each vigilance state: Drowsy, Sleep (SWS+REM) and Wake across the seasons, plotted separately for light (yellow background) and dark (gray background). Horizontal lines within boxes denote medians (50^th percentile); horizontal edges of the boxes denote the 25^th and 75^th percentiles; whiskers extend to the 5^th and 95^th percentiles. Open symbols show the outliers. Figure 3B. States of vigilance as a function of light and dark in the four seasons. The percentage of time in each state is shown (colored circle) for each bird in the light (yellow background) and in the dark (gray background). The seasonal average of all birds is plotted at the endpoints of the lines. Lines highlight the change in vigilance state expression from light to dark during winter (blue) and summer (red), and the relative lack of change in spring (green) and fall (brown). Note that the length of the dark period varies with the season so equal percentages do not reflect equal times.

Figure 4

Sleep consolidation index for all seasons. Hourly average ratio of sleep bout length to wake bout length was calculated for birds during each season. The blue line represents a smoothed curve through these data. The time during which the smoothed value of the ratio of sleep bout length to wake bout length exceeded 1.00 was used to define the "sleep consolidation index" for each season. In winter, hour 10 is first hour in which the ratio exceeds 1 and this ratio falls below 1 at hour 21, resulting in a sleep period of 11 hours. In summer, the sleep period begins at hour 18 and ends at hour 23. It is noteworthy that this sleep period begins prior to the onset of darkness. A similar phenomenon can be observed in the sleep times plotted in Figure 2. There was no sleep consolidation during the migratory seasons, spring and fall.

Figure 5

Box-and-whisker plots illustrating DRL performance during each season. Top shows response rate (responses/minute) and bottom shows the behavioral inhibition ratio (reinforcers/responses). Horizontal lines within boxes denote medians (50^th percentile); horizontal edges of the boxes denote the 25^th and 75^th percentiles; whiskers extend to the 5^th and 95^th percentiles. Open symbols show the outliers. N = 15. Response rates are significantly higher during the migratory periods relative to the non-migratory periods and the behavioral inhibition ratio was significantly lower during migration. Operant data were analyzed for the same weeks, except in fall when operant animals were exposed to photoperiods ranging from 16.0:8LD - 11.5:12.5LD.

Figure 6

Cumulative records for an individual bird from a single session during each season. Diagonal lines extending directly beneath the record (hash marks) indicate food reinforcement. Note there are no reinforcements earned during the spring season. Vertical lines extending from 100 to 0 responses (spring and fall only) are resets of the "pen" due to high rates of responding; this was done to keep the scale constant across each of the four records.

Figure 7

Performance within sessions on the Differential Reinforcement of Low Rate (DRL) task. Mean ± SEM (n = 15) of number of responses (left axis, dotted lines) and number of reinforcers (right axis, solid line) are plotted for each 3 minute period in the 30 m session.

Figure 8

Relative frequency distribution of interresponse times (IRTs) using a bin size of 2 seconds averaged across birds in each season. Dashed line indicates the time at which IRTs were reinforced. Proportion of reinforced IRTs, those which occur after the 20 second delay, is shown to the right of the dashed line. IRT distributions are typically bimodal, with the most IRTs either short or long enough to be reinforced. N = 15. Error bars represent the 95% CI.

Figure 9

48 hour sleep deprivation with the DRL birds. Top shows response rate (responses/minute), center shows number of reinforcers acquired, and bottom shows the behavioral inhibition ratio (reinforcers/responses). Data shown are organized by season, Sleep deprivation decreased response rate regardless of season. The letters a, b, and c indicate statistical differences between DRL performance during the sleep deprivation compared to Pre Sleep Deprivation. Pre Sleep Deprivation performance did not differ statistically from Recovery or Post Recovery for any season, although average response rates during Post Recovery were about 25% (Winter) or 50% (Spring) higher than during Pre Sleep Deprivation. N = 15. Error bars represent half of the 95% CI.