Characterizing behavioral sleep using actigraphy in adult dogs of various ages fed once or twice daily

doi:10.1016/j.jveb.2012.10.007

Journal of Veterinary Behavior

Volume 8, Issue 4, July–August 2013, Pages 195-203

https://doi.org/10.1016/j.jveb.2012.10.007 Get rights and content

Abstract

Adult dogs possess strong diurnal locomotor activity/rest rhythms, and sleep/wake patterns have been characterized. However, behavioral sleep/wake data are lacking related to aging and daily feeding pattern. Three groups (young adults [Y], 1.5–4.5 years; middle-aged adults [M], 7–9 years; and senior, 11–14 years) of beagles (N = 48) wore the Actiwatch activity monitoring system (Respironics Co., Inc., Bend, OR) for 3 days while housed indoors with 12-hour light/dark schedule and fed once or twice daily. Actiware-Rhythm software (version 5.52; Respironics Co., Inc., Bend, OR) was used to estimate behavioral sleep or wake from locomotor activity data. All dogs demonstrated diurnal sleeping patterns. Total wake minutes during the light phase declined with age (P < 0.05) and differed by 7.7% and 10.2% for middle-aged adults and seniors, respectively, compared with young adults. Further analysis revealed that increased light phase nap bouts (P < 0.008), not increased nap duration, caused this decline. Total sleep minutes during the night increased with age, as middle-aged adults and seniors slept at least 38 (P = 0.01) more minutes than young adults. Increased sleep time at night resulted from a longer sleep interval duration (P = 0.05), delayed morning activity onset time (P = 0.02), and marginally fewer waking bouts (P = 0.07). Independent of age, twice-daily feeding significantly influenced daytime sleeping patterns but did not affect total minutes recorded as sleep during the day. Interestingly, napping bouts decreased significantly (P = 0.01) and napping duration increased (P = 0.0001) when fed twice-daily. Twice-daily feeding was also associated with earlier sleep onset time at night and onset of morning activity, as well as shortened sleep interval. Clear changes in behavioral sleep patterns were observed with age and daily feeding schedule.

Introduction

Normal aging is associated with an increased prevalence in sleep disturbances and decreases in sleep quality. Aging is also associated with modifications in locomotor activity and circadian rhythms, as well as neutered (altered) food intake patterns. Both photoperiod and food availability entrain circadian rhythms in mammals, but function independently, as food-anticipatory activity rhythms set by daily feeding schedules are not under control by the light-entrainable circadian pacemaker located in the suprachiasmatic nuclei (SCN) of the hypothalamus (Froy, 2007; Mistlberger, 2011). Aging and many neurodegenerative diseases like Alzheimer disease have links to dysregulation of the SCN (Weldemichael and Grossberg, 2010), yet the influence of aging on neurological processes that control food-anticipatory behaviors is poorly understood. Therefore, it is not clear how different feeding regimens influence circadian sleep/wake patterns in aged mammals, particularly in dogs.

As many as 80% of elderly people experience difficulty initiating sleep, increased night-time wakefulness, early waking, and/or increased daytime napping (Foley et al., 1995; Wolkove et al., 2007). Likewise in dogs, aging has been associated with changes in sleep patterns (Takeuchi and Harada, 2002), and neutered sleep/wake cycles have been reported by pet owners (Houpt, 1998; Bain et al., 2001; Neilson et al., 2001). Previous work has established that healthy adult dogs show a clear circadian rhythm for sleep/wake patterns (Lucas et al., 1977; Gordon and Lavie, 1984; Takeuchi and Harada, 2002) and primarily exhibit high daytime locomotor activity/rest patterns to establish dogs as diurnal mammals (Tobler and Sigg, 1986; Nishino et al., 1997; Siwak et al., 2003; Zanghi et al., 2008; Zanghi et al., 2012).

Polysomnography (PSG) is considered to be the “gold standard” in determining sleep/wake status. More recently in people, accelerometer devices that detect locomotor activity are being used to generate actigraphy-estimated sleep data as an alternative to PSG-generated sleep (Morgenthaler et al., 2007; Walters et al., 2007; Mehra et al., 2008) and also with nonhuman primates (Sri Kantha and Suzuki, 2006; Suzuki and Sri Kantha, 2006; Sri Kantha et al., 2009). Behavioral sleep measured by actigraphy has now been used to study sleep/wake rhythms in people for more than 2 decades (Ancoli-Israel et al., 2003; Morgenthaler et al., 2007; Blackwell et al., 2008, Blackwell et al., 2011). In canines, the simultaneous use of PSG and actigraphy was performed. Consequently, comparison of actigraphic measures and PSG-recorded sleep states were made using the MiniMitter Actiwatch device (Minimitter, Inc., Sundriver, OR) (John et al., 2000). This comparison was used to determine wake thresholds and demonstrated that actigraphy-generated sleep/wake data in narcoleptic dogs have a strong correlation with PSG-defined wake and sleep (John et al., 2000). Subsequent work from this laboratory has reported additional actigraphic-estimated sleep data in narcoleptic and control dogs (Wu et al., 2002; Boehmer et al., 2004). However, this body of research did not characterize or report the sleep/wake statistics in normal control dogs such as estimates of duration and bouts of daytime and night-time sleep. Therefore, a comprehensive characterization of actigraphy-generated behavioral sleep/wake data and behavioral sleep variables described previously in healthy adult dogs is still needed.

Our previous research demonstrated that locomotor activity patterns change with age and daily feeding frequency (Zanghi et al., 2012). Therefore, this study sought to use this locomotor activity data to generate behavioral sleep or wake status data using actigraphy. The purpose of the present study was 2-fold. First, to uniquely characterize behavioral sleep in healthy dogs using actigraphy recorded with an ambulatory activity monitoring device, specifically the MiniMitter Actiwatch system that was previously validated to evaluate behavioral sleep (John et al., 2000). The second goal was to assess age-related changes in actigraphy-generated sleep statistics and simultaneously evaluate these sleep statistics relative to daily feeding frequency. Consequently, an initial characterization of sleep patterns in adult and aged dogs based on actigraphy was performed, while also reporting changes relative to age and daily feeding pattern on several sleep statistics; such as daytime napping bouts and duration, night-time waking bouts and duration, sleep efficiency, morning activity onset time, and sleep onset latency.

Section snippets

Animals, housing, and feeding regimen

Adult beagle dogs (N = 48) were divided into 3 age groups: young (1.5–4.5 years; N = 16), middle age (7–9 years; N = 16), and senior (11–14 years; N = 16). The dogs were housed in groups of 2–4 per run (5 feet wide × 15 feet in length) based on compatibility and sex, and all dogs were housed in the same kennel location with ability to see other dogs in adjacent and opposing runs. Each dog had direct interaction with caretaker staff on daily basis and had access to toys.

In their normal housing,

Results

Actigraphy-generated behavioral sleep/wake statistics were determined for 3 consecutive 24-hour periods to characterize age-related changes in sleep and wake patterns while on a once- or twice-daily feeding schedule. A repeated-measures ANOVA revealed that no age × feeding frequency or 3-way interactions were observed for all sleep/wake statistics analyzed, but there were several significant main effects of age or feeding frequency. The main effects of age or feeding frequency are described

Discussion

The current findings present 3 sets of novel data. The first is the characterization of behavioral sleep and wake patterns in healthy dogs based on actigraphy data, and the second is the characterization of age differences in canine behavioral sleep/wake patterns, which is not based on electroencephalographic recordings. Third and finally, we document how different daily feeding regimens influence sleeping patterns in animals fed once per day with patterns in the same animals fed twice per day.

Conclusions

Having quantifiable and objective measures of particular canine sleep/wake behaviors, associated not only with advancing age but also exaggerated behaviors associated with particular neurological deficits, should improve our understanding of neuropsychological processes and disease states in dogs. This is particularly germane in light of an entire body of work documenting deficits in canine cognition and aging (Milgram et al., 1994, Milgram et al., 2006, Milgram et al., 2010). Cognitively

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ResearchCharacterizing behavioral sleep using actigraphy in adult dogs of various ages fed once or twice daily

Abstract

Introduction

Section snippets

Animals, housing, and feeding regimen

Results

Discussion

Conclusions

Clin. Cornerstone

Exp. Neurol.

Clin. Geriatr. Med.

Front. Neuroendocrinol.

Physiol. Behav.

Epilepsy Behav.

Physiol. Behav.

Ageing Res. Rev.

Physiol. Behav.

Electroencephalogr. Clin. Neurophysiol.

Neurosci. Res.

Neurobiol. Aging

Physiol. Behav.

Neurosci. Lett.

Behav. Brain Res.

Exp. Gerontol.

Electroencephalogr. Clin. Neurophysiol.

The role of actigraphy in the study of sleep and circadian rhythms

Sleep

Insomnia and daytime napping in older adults

J. Clin. Sleep Med.

Actigraphy

Respir. Care Clin. N. Am.

Predicting behavioral changes associated with age-related cognitive impairment in dogs

J. Am. Vet. Med. Assoc.

Comparison of sleep parameters from actigraphy and polysomnography in older women: the SOF study

Sleep

Factors that may influence the classification of sleep-wake by wrist actigraphy: the MrOS Sleep Study

J. Clin. Sleep Med.

Sleep complaints among elderly persons: an epidemiologic study of three communities

Sleep

Domestic Animal Behavior for Veterinarians and Animal Scientists

Research
Characterizing behavioral sleep using actigraphy in adult dogs of various ages fed once or twice daily