Possible association between spindle frequency and reversal-learning in aged family dogs

Abstract

In both humans and dogs sleep spindle occurrence between acquisition and recall of a specific memory correlate with learning performance. However, it is not known whether sleep spindle characteristics are also linked to performance beyond the span of a day, except in regard to general mental ability in humans. Such a relationship is likely, as both memory and spindle expression decline with age in both species (in dogs specifically the density and amplitude of slow spindles). We investigated if spindle amplitude, density (spindles/minute) and/or frequency (waves/second) correlate with performance on a short-term memory and a reversal-learning task in old dogs (> 7 years), when measurements of behavior and eeG were on average a month apart. Higher frequencies of fast (≥ 13 Hz) spindles on the frontal and central midline electrodes, and of slow spindles (≤ 13 Hz) on the central midline electrode were linked to worse performance on a reversal-learning task. The present findings suggest a role for spindle frequency as a biomarker of cognitive aging across species: changes in spindle frequency are associated with dementia risk and onset in humans and declining learning performance in the dog.Sleep spindles are brief trains of rhythmic activity, at least half a second in duration 1 and maximally 6 seconds long 2 , which appear in the EEG signal of humans 3,4 and other mammals 5 during non-REM sleep, in particular stage 2 of non-REM sleep in humans. They are commonly distinguished in a slow (predominantly frontal, ≤ 13 Hz) and fast (≥ 13 Hz, predominantly central and posterior) subtype 6 .One promising model animal in comparative sleep spindle research is the dog (Canis familiaris). A shared anthropogenic environment and evolutionary adaptation to its dynamics 7 characterize dogs as an animal model for human conditions in general 8 , and they have specifically been argued a favorable model in comparative neuroscience as well 9 . Moreover, there is recent evidence 10,11 that, in dogs, transients oscillating in the 9-16 Hz frequency range, corresponding to the broad definition of the sigma band or spindling frequency in humans 12,13 , are analogous to human sleep spindles (See Table 1 for an overview of these analogies and the associated literature).As a note of caution, regarding spindle-cognition associations in general, detection methods for sleep spindles tend to correlate poorly with each other 14,15 which is challenging to the comparability between studies. In addition, sleep spindles also appear to display a link to memory consolidation and learning only under specific circumstances. The distance of the to-be-learned material to prior knowledge 16,17 , the exact stage of non-REM sleep in which spindles are measured 18 and the timing relative to cortical up-states and ripples 17-19 all seem to have an influence. In light of this it is not surprising that associations between sleep spindles and learning are not always replicated 20 . Considering the controversy about the comparability of different spindle detection m...

Reliability of Family Dogs’ Sleep Structure Scoring Based on Manual and Automated Sleep Stage Identification

“…The relative spectral power of the Fz channel for all sleep stages (D, NREM and REM) was compared between Coder 1 (A + B) and Coder 2, as well as between 1 and 4 channel scoring by Coder 2, with paired t-tests, separately for the four frequency ranges of delta (1-4 Hz), theta (4-8 Hz), alpha (8-12 Hz) and beta (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30).…”

“…In spite of these limitations, high agreement between expert scorers was found for the identification of NREM ( Table 3 , Table 4 and Table 5 ). Some of the more recent work on dog PSG data exclusively examines NREM traces [ 24 , 26 , 39 ], while comparisons of the relative ratio of REM to NREM duration [ 4 , 30 ] are also relatively safe from the difficulty of distinguishing D from W. This suggests that visual scoring in the dog can be sufficient with regard to many questions.…”

“…Coder 1A (V Reicher), the most experienced rater who had already scored more than 200 canine PSG recordings in the past, scored four out of the ten recordings (originally included in [25]). Coder 1B (I Iotchev), the least experienced rater, who had scored approximately 50 PSG recordings so far, scored six out of the ten recordings (originally included in [26]). Coder 2 (A Gergely), who was in between Coder 1A and 1B regarding expertise, had scored approximately 110 canine PSG recordings in the past and coded all ten recordings twice (both with one and four EEG channels visible).…”

Gut Microbiome Composition is Associated with Age and Memory Performance in Pet Dogs

“…Companion dogs (N = 29, 14 males, age range: 3 to 13-year-old, mean age (SD): 9.7 (2.6) years, mean weight (SD): 23.3 (14.3) kg; 1 Bernese mountain dog, 6 Border collies, 2 Cairn terriers, 1 German wirehaired pointer, 1 Labrador retriever, 12 Mixed breeds, 1 Moscow watchdog, 2 Vizslas, 3 Whippets) living in Hungarian households were included in the study. The dogs participated in a larger study investigating the behavioral signs of aging [27]. These dogs had defecated right after the behavior tests and were thus included here due to the availability of fecal samples.…”

“…The detailed procedure of the behavior test is described in [27,32]. In short, five identical, open containers were positioned in equal distance from each other in a semi-circular arrangement, each container being two meters away from the starting position of the dog.…”