The effect of altering routine husbandry factors on sleep duration and memory consolidation in the horse

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Highlights

  • Sub-optimal bedding and lighting conditions significantly affect equine recumbency and associated sleep stages.

  • Reduced recumbent sleep state duration appears compensated for by increased time standing (associated with NREM sleep state).

  • Reduction in sleep duration appears to have some effect on cognitive performance.

Abstract

Sleep is a critically important behaviour for all mammals due to its fundamental role within homeostatic/circadian systems and memory consolidation. As a large and vigilant prey species that is highly sensitive to stimuli at night, the horse sleeps less than other mammalian species. For this reason, the domestic environment has the potential to greatly affect the duration and quality of equine sleep. This study aimed to determine the effect of environmental factors on equine sleep stages, and whether this would influence cognitive performance during a spatial memory task. Ten riding school horses (mixed breed/ height/ sex; average age 14.9 + 2.4 years) were randomly assigned to two groups (n = 5) within a five-week crossover repeated measures design experiment. Each group experienced a combination of one of two light conditions (lights on = Treatment; lights off = Control), and one of two bedding depth treatments (15 cm bed = control; 5 cm bed = treatment) for six days. Duration of sleep stage behaviours (standing Non-Rapid Eye Movement [NREM]), sternal NREM, sternal Rapid Eye Movement [REM] and lateral REM) were measured continuously using CCTV infrared cameras. For the spatial memory task, latency, number of correct responses, and differences between these parameters during training and testing days were measured. A repeated measures general linear model assessed the effects of treatment conditions on duration of sleep stage, and changes in sleep stage over time (bedding and light set as within-subject factors). Wilcoxon Signed-Rank and paired t-tests determined differences in memory task parameters between treatments. Comparing Treatment Bedding with Control Bedding conditions, horses spent on average significantly less time in lateral REM (0.34 ± 0.12 versus 0.46 ± 0.13 h; p = 0.032) and sternal NREM (0.64 ± 0.10 versus 0.80 ± 0.12 h; p = 0.007), and significantly more time in standing NREM (3.69 ± 0.76 versus 3.17 ± 0.77; p = 0.024). Only sternal REM was significantly affected during the Treatment Light condition compared to control conditions (0.53 ± 0.07 versus 0.67 ± 0.11; p = 0.031). Interactions between day and treatment were apparent for specific sleep stage behaviours indicative of acclimatisation. No significant effects (p > 0.05) of Treatment Light or Bedding conditions were detected for performance during the spatial memory test. Overall, horses exposed to sub-optimal conditions tended to display significantly less time in recumbent sleep stages (NREM and REM) and increased time in a standing NREM stage. The impact of reduced sleep on equine cognition requires further study.

Introduction

Sleep is one of the most critically important behaviours to all domestic animals due to its fundamental role within homeostatic and circadian systems (Toth and Bhargava, 2013). Both of the primary sleep stages (Non-Rapid Eye Movement [NREM] and Rapid Eye Movement [REM]) regulate a range of physiological processes including neuroendocrine modulation, restorative functions, and memory consolidation (Beccuti and Pannain, 2011; Mavanji et al., 2012; Toth and Bhargava, 2013). Thus, reduced sleep and states of sleep deprivation cause changes in a range of cognitive, emotional and physiological states such as cognitive impairment including reduced spatial memory (Guan et al., 2004), increased levels of anxiety and aggression, and depletion of glycogen stores along with changes in appetite (McEwen, 2006).

The ability of animals to sleep is affected by their environment, for example, different light and temperature conditions affect the duration and type of sleep (via changes in melatonin levels) in a range of animal species (Redlin, 2001; Gooley et al., 2011; Siegel, 2005). For prey species, the perceived risk of predation is also influential on the amount of sleep that the animal experiences (Lima et al., 2005), which is greatly affected by the size of the animal and its ability to access secure sleep locations within its environment. Larger species, for example, tend to be more exposed within their environment and therefore display higher levels of vigilance throughout the night (Allison and Cicchetti, 1976). This can also lead to a greater potential disruption of sleep in these species when exposed to novel stimuli during sleep periods (Campbell and Tobler, 1984).

The horse is an example of a large prey species that engages in less sleep compared to other mammalian species for the previous reasons identified (Siegel, 2005). On average the horse achieves 3.82 h for total sleep time (2.88 h NREM and 0.63 h REM) within a 24 h period (Greening and McBride, in preparation (Greening and McBride, 2021). However, unlike other large herbivores, the horse sleeps for relatively small amounts of time in the recumbent position tending to achieve the majority of sleep whilst standing (average 21 % vs. 79 %, respectively) (Dallaire, 1986). This can be reduced further if the horse is not habituated to the environment (Ruckebusch et al., 1970). Whilst the horse is able to achieve NREM sleep in both standing and recumbent positions, REM sleep can only be effectively achieved during recumbency due to the muscle atonia that occurs within this sleep stage (Ruckebusch et al., 1970). Thus, reluctance of the horse to enter the recumbent position within the stable can have a welfare and performance effect due to a reduction in REM sleep.

Other factors within the domestic environment can potentially affect horses’ ability to adopt a recumbent position for the purpose of sleep. For example, the average duration of laterally recumbent behaviour is reportedly higher for straw bedding (44.0 min) compared to shavings and/or straw pellets (21.6 min) (Pedersen et al., 2004; Greening et al., 2013; Werhahn et al., 2010) with bedding depth also being important in this respect (Pedersen et al., 2004; Werhahn et al., 2010; Modena and Greening, 2019). Although no research has been directly carried out on the effect of lighting conditions on equine sleep stages, light (between 3 and 10 lx) is known to affect melatonin production in the horse (Walsh et al., 2013). Thus, artificial lighting within the stable environment will undoubtedly have an effect on the animal's ability to enter into stages of sleep. Traditional practice is that artificial lights are turned off within the stable environment overnight, however, in some instances this may not always be the case. In addition, late-night checks on horses involving lights being turned on could affect melatonin cycles and subsequently, sleep patterns.

The aim of this study was to determine the effects of altering the environment (bedding depth and light) on the duration of different sleep stages (NREM and REM) in the stabled horse. In addition, to determine the functional and welfare consequences of potential sleep deprivation, the study also assessed the effects of bedding depth and light on performance within a spatial memory task.

Section snippets

Animals

Ten school horses (6 geldings, 4 mares; mixed breeds; average age 14.9 +2.4 years; average height 163.5 +7.4 cm, none displaying stereotypic behaviours) were observed in their usual 3.6m × 3.6m stable, experiencing the same feeding schedule (three forage rations presented morning, midday and evening) and similar amounts of exercise, all stabled on the same yard at Aberystwyth University. During the study, subjects were routinely stabled for 24 h Monday to Friday then turned out to pasture for

Mean duration

During the Light (lux 2) and Bedding (15 cm) control condition, horses slept for an average of 5.18 ± 0.88 h with an average of 3.94 ± 0.85 h (76.1 %) and 1.4 ± 0.13 h (23.9 %) spent in NREM and REM sleep stages respectively. There was no significant effect (F(1,9) = 0.01, p = 0.76) noted for Control Bedding (5.19 ± 0.78 h) versus Treatment Bedding (5.10 ± 0.82 h) or the Control Light (F(1,9) = 0.45, p = 0.52) (5.26 ± 0.77 versus the Treatment condition (5.04 ± 0.84 h) on the total amount of

Baseline sleep values and variability

Horses slept on average for a total of 5.2 ± 0.88 h/day during the Control conditions week (15 cm bedding, lights off), which is higher than has been previously reported for total sleep time (TST) for horses (Zepelin, 2000; Wohr et al., 2016). Whilst the use of behavioural observations to quantify equine sleep stages comes with a risk of over or under estimating time spent in each sleep stage, the equine sleep positions observed in this study aligned strongly with the descriptions and

Conclusion

The duration of equine sleep stages was found to be affected by both the depth of bedding and lighting conditions. During sub-optimal conditions horses tended to display significantly reduced time in recumbent states for both NREM and REM sleep, which was compensated by increased time in the standing NREM stage. The impact of reduced sleep on the animal was not fully determined in this study. Although the data suggested that there might be some effect on spatial memory, a more cognitively

Author Declaration Template

We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

We confirm that the manuscript has been read and approved by all named authors and that there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us.

We confirm that we

Acknowledgements

We would like to thank Hannah Appleton, Jennifer Lawrence and Caryl Thomas at LLuest Riding Centre for aiding and supporting the day-to-day running of the research trial. We would also like to thank Dr Matthew Parker at the University of Portsmouth for his guidance on adapting the spatial memory task for use in horses.

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