Abstract
Non-REM bursts of activity in the sigma range (9–16 Hz) typical of sleep spindles predict learning in dogs, similar to humans and rats. Little is known, however, about the age-related changes in amplitude, density (spindles/minute) and frequency (waves/second) of canine spindles. We investigated a large sample (N = 155) of intact and neutered pet dogs of both sexes, varying in breed and age, searching for spindles in segments of non-REM sleep. We recorded EEG from both a frontal midline electrode (Fz) and a central midline electrode (Cz) in 55.5% of the dogs, in the remaining animals only the Fz electrode was active (bipolar derivation). A similar topography was observed for fast (≥13 Hz) spindle occurrence as in humans (fast spindle number, density on Cz > Fz). For fast spindles, density was higher in females, and increased with age. These effects were more pronounced among intact animals and on Fz. Slow spindle density declined and fast spindle frequency increased with age on Cz, while on Fz age-related amplitude decline was observed. The frequency of fast spindles on Fz and slow spindles on Cz was linked to both sex and neutering, suggesting modulation by sexual hormones. Intact females displayed higher frequencies than males and neutered females. Our findings support the argument that sigma bursts in the canine non-REM sleep are analogous to human sleep spindles, and suggest that slow and fast spindles display different trajectories related to age, of which an increase in frontal fast spindles is unique to dogs.
Highlights
The sleeping brain shows various patterns of activity that predict awake performance in the domains of memory and cognitive ability[1]
Using criteria for automatic sleep spindle detection previously validated in humans[17] we were able to show that transients in the sigma range (9–16 Hz), characteristic of the human sleep spindle, show a similar association with post-sleep recall of novel information, i.e. dogs with higher learning gain displayed more spindles/minute[18]
A positive correlation between spindle occurrence and memory performance, for instance, can be observed with[38,39] and without[40,41,42] separating spindles into ‘slow’ and ‘fast’, whereas many findings on development[19,20] and sexual dimorphism[43] are specific for the different subtypes, e.g. a rise in spindle density during adolescence appears to be specific for fast spindles[19]
Summary
The sleeping brain shows various patterns of activity that predict awake performance in the domains of memory and cognitive ability[1] Several of these oscillatory activities are altered in the aging process[2], which makes sleep physiology an attractive target for studying cognitive aging in humans and animal models. A positive correlation between spindle occurrence and memory performance, for instance, can be observed with[38,39] and without[40,41,42] separating spindles into ‘slow’ and ‘fast’, whereas many findings on development[19,20] and sexual dimorphism[43] are specific for the different subtypes, e.g. a rise in spindle density during adolescence appears to be specific for fast spindles[19]
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