Effect of sleep loss on executive function and plasma corticosterone levels in an arctic-breeding songbird, the Lapland longspur (Calcarius lapponicus)

Highlights

• Sleep fragmentation significantly elevated corticosterone levels.

• Color association test accuracy was significantly greater in treatment individuals.

• No effect of treatment on color association test completion time.

• No effect of treatment on spatial learning test, body mass, or satiety.

• Longspurs exhibited behavioral, but not physiological, resilience to sleep loss.

Abstract

Sleep is a fundamental component of vertebrate life, although its exact functions remain unclear. Animals deprived of sleep typically show reduced neurobiological performance, health, and in some cases, survival. However, a number of vertebrate taxa exhibit adaptations that permit normal activities even when sleep is reduced. Lapland longspurs (Calcarius lapponicus), arctic-breeding passerine birds, exhibit around-the-clock activity during their short breeding season, with an inactive period of ca. 4 h/day. Whether behavioral or physiological costs occur from sleep loss (SL) in this species is unknown. To assess the effects of SL, wild-caught male longspurs were placed in captivity (12L:12D) and trained for one month to successfully learn color association and spatial memory tasks. Birds were then placed in automated sleep fragmentation cages that utilize a moving wire to force movement every 1 min (60 arousals/h) during 12D (inactive period) or control conditions (during 12L; active period). After SL (or control) treatment, birds were presented with color association and spatial memory tasks a final time to assess executive function. Baseline plasma corticosterone concentration, body mass, and satiety were also measured. SL significantly elevated corticosterone levels and increased accuracy during color association recall but did not affect the overall time required to complete the task. SL had no effect upon spatial memory, body mass, or satiety. Taken together, these results suggest that Lapland longspurs exhibit a degree of behavioral, but not physiological, insensitivity to acute SL. Whether elevated plasma concentrations of corticosterone play a direct role in ameliorating cognitive deficits from SL require additional study.

Introduction

Sleep is a fundamental component of vertebrate life and is generally defined as a rapidly reversible state of reduced responsiveness to external stimulation, motor activity, and metabolism (Siegel, 2009; Chokroverty, 2017). However, the precise functions of sleep have produced considerable debate. Although sleeping accounts for nearly one-third of a human's life, the benefits associated with the recommended 7–9 h of sleep per night (Hirshkowitz et al., 2015) can be assessed only when sleep is prevented. Moreover, mounting evidence suggests that sleep is critical to learning and memory (Stickgold, 2005; Diekelmann and Born, 2010), and when sleep is disrupted, memory functions consequently diminish (Walker and Stickgold, 2006; Goel et al., 2009). In mice, disruption of sleep can significantly decrease performance on a series of executive function tasks such as novel object recognition (Palchykova et al., 2006; Rolls et al., 2011) and food-motivated reaching (Vyazovskiy et al., 2011). In humans, significantly decreased reaction times on psychomotor vigilance tasks (Kribbs and Dinges, 1994) as well as deteriorated decision-making skills (Harrison and Horne, 2000) have been observed.

The detrimental effects associated with sleep loss (SL), however, do not necessarily hold true when applied to other species throughout the animal kingdom. For example, although some insects display periods of inactivity, they fail to meet the behavioral definition of sleep despite having functional nervous systems (Siegel, 2008). Among mammals, time spent sleeping is quite variable, ranging from fewer than 3 h (e.g., elephants, giraffes) to >20 h per day (e.g., some bat species, opossum) (Zepelin et al., 2005; Siegel, 2009). The walrus undergoes a period of extended wakefulness for several days (Pryaslova et al., 2009) while dolphins and whales undergo unihemispheric slow-wave sleep (Lyamin et al., 2004) in which the other hemisphere of the brain displays electrophysiological correlates of wakefulness.

Birds are of particular interest when investigating the detrimental effects of SL due to their variability in behavioral and physiological responses to SL. For example, European starlings (Sturnus vulgaris) exhibit improved memory consolidation to an acoustic stimulus when permitted to sleep (Brawn et al., 2010). In contrast, white-crowned sparrows (Zonotrichia leucophrys gambelii) reduce average sleep duration by 60% during migration, but no deficits in learning or performance are documented relative to non-migratory periods (Rattenborg et al., 2004). However, when exposed to 48 h of experimental SL, this species exhibits decrements in executive function and this effect is conserved across major life-history stages (e.g., breeding, non-breeding, spring and fall migration; Jones et al., 2010).

Around the summer and winter solstices, animals that reside in Antarctica or north of the Arctic circle (>66°33′) experience weeks to months of either continuous daylight or darkness, respectively (Pielou, 1994). For humans, constant light during the summer, as well as constant darkness in the winter, can alter sleep patterns and disrupt the circadian clock (Arendt, 2012). For example, polygynous pectoral sandpipers (Calidris melanotos) that breed in the Arctic exhibit “around-the-clock” activity that corresponds with high electromyogram activity and wakefulness (Lesku et al., 2012). It has been proposed that intense competition for mates leads to “reproductive sleeplessness,” as evidenced by the most active males siring a greater number of offspring (Lesku et al., 2012).

The family Calcariidae is an avian clade that includes arctic-breeding specialists with circumpolar distributions (Hussell and Montgomerie, 2002; Montgomerie and Lyon, 2011), such as Lapland longspurs (Calcarius lapponicus) and snow buntings (Plectrophenax nivalis). Due to the short summer season at high latitudes, breeding is restricted to 5–6 weeks and is highly synchronized. Within this short season, pairs must be successful in accomplishing a number of breeding substages such as territory establishment, pair bonding, nesting, and parental care. Pairs only have time to produce one clutch, and re-nesting is only possible early in the season (Custer and Pitelka, 1977; Pielou, 1994). Any failure or disruption of one of these substages can reduce annual reproductive success to zero (Wingfield et al., 2004; Chmura et al., 2018). Previous studies indicate that male Lapland longspurs on their breeding grounds in Barrow, Alaska (71°N) spend approximately 20 h per day exhibiting behaviors associated with activity across a 24-h polar day (Custer et al., 1986; Ashley et al., 2013). If longspurs exhibited impairments associated with SL as previously reported in other birds (e.g., Brawn et al., 2010; Jones et al., 2010), then we would predict severe disadvantages on their arctic breeding grounds where they compete for territory, resources, and mates.

Many birds in energetically demanding conditions exhibit elevated levels of corticosterone, a steroid hormone produced from the adrenal gland (Wingfield et al., 1997). Moreover, zebra finch (Taeniopygia guttata) exhibit increased basal levels of plasma corticosterone in response to 12 h of experimental SL (Cooper et al., 2019). A number of animal studies have demonstrated that short-term increases in glucocorticoid concentrations are beneficial to learning and memory whereas high and chronic levels have negative effects upon cognition through increasing neuronal cell death and decreasing neurogenesis (reviewed in Sapolsky et al., 2000). For example, acute injections of corticosterone in mountain chickadees (Poecile gambeli), a food-storing bird, increased retrieval efficiency of caches compared with vehicle (Saldanha et al., 2000). Interestingly, moderate chronic elevation of corticosterone levels, via the use of subcutaneous implants, still enhanced cache retrieval and improved spatial memory performance in this species (Pravosudov, 2003). Given that glucocorticoid stress responses are positively correlated with latitude (Bókony et al., 2009), and that Lapland longspurs breeding in a high-arctic environment (e.g., Thule, Greenland, 76°N) exhibit more robust adrenocortical responses to stress than longspurs breeding at low-arctic sites (e.g., Toolik field station, Alaska 68°N; Walker et al., 2015), it is possible that SL-induced elevation in glucocorticoids could play a role in mediating executive function performance in passerines breeding at high latitudes.

The aim of this study was to investigate whether experimental acute SL of captive longspurs in breeding condition exacts a physiological response, such as increased plasma corticosterone concentration, and a behavioral response, such as decreased cognitive performance on a series of executive function tasks. In this case, we would predict 12 h of SL to significantly increase corticosterone concentrations and decrease cognitive performance relative to controls, suggesting that longspurs are sensitive to the effects of SL. However, given the around-the-clock activity of free-living longspurs, it is possible that 12 h of SL would result in no physiological or behavioral responses to SL, which would yield no change in cognitive performance and no increase in plasma glucocorticoid levels (the null hypothesis), suggesting physiological and behavioral resilience. Finally, if elevated corticosterone directly enhances cognition in longspurs, then an elevation in plasma corticosterone from SL could potentially ameliorate or buffer any cognitive deficits from SL, leading to no alterations in executive function, or even enhancement.