Age-related differences and sexual dimorphism in canine sleep spindles

Iotchev, Ivaylo Borislavov; Kis, Anna; Turcsán, Borbála; Lara, Daniel Rodrigo Tejeda Fernández de; Reicher, Vivien; Kubinyi, Enikő

doi:10.1038/s41598-019-46434-y

Cited by 31 publications

(54 citation statements)

References 67 publications

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“…For analyses distinguishing fast and slow spindles, the final count of spindling events is separated into slow and fast spindles using 13 Hz as a cut-off value (as in Schabus et al 40 and Hahn et al 30 ), that is, detections with frequency ≤ 13 Hz is categorized as slow, ≥13 Hz -fast. The frequency of slow and fast spindles overlaps at 13 Hz (see also histogram of population sigma frequency distribution for dogs on Fz and Cz in Iotchev et al 11 ). The mean amplitude of a recording was calculated as the average across spindle detections in that recording of the root-mean-square value for the signal segments corresponding to spindling events.…”

Section: Spindle Detectionmentioning

confidence: 95%

“…The method used to detect spindles is described in Iotchev et al 10,11 and uses criteria proposed by Nonclercq et al 44 . Importantly, the method makes use of a two-step procedure and a spectral analysis with a moving, overlapping time-window of 0.5 seconds length (the minimum duration of spindles 1 ).…”

Section: Spindle Detectionmentioning

confidence: 99%

“…The sample from which the present selection of dogs was taken (based on the availability of EEG data) was demonstrated before to display a variability in cognitive performance 23,47 . We hypothesized that occurrence, measured as density (spindles/minute), and/or amplitude would show a positive association with performance on the two tasks, while we expected an inverse relationship with spindle frequency, as it rises with age in humans 29,33,48 and dogs 11 . Importantly, as done in many human studies, we separately analyzed fast and slow spindles 10,11 as in both humans and dogs age-related changes in spindle characteristics differ between the slow and fast variety and topographically (for instance more pronounced slow spindle amplitude decline over the frontal cortex in both humans and dogs 11,25,26 ).…”

mentioning

confidence: 96%

“…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 methods 14,15 , it is important to note that both studies to date on spindle expression in dogs (Iotchev et al 10,11 ) used the same search criteria. The two studies are therefore directly comparable with each other and the present study.…”

mentioning

confidence: 99%

“…In the present study we apply the same automatic spindle detection algorithm as previously used in the dog 10,11 to a data-set containing two measurements per dog, of each EEG and behavior (a short-term memory task and a reversal-learning paradigm) to evaluate whether canine spindles are useful markers of cognitive aging. First, we Table 1.…”

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

Iotchev

Szabó

Kis

et al. 2020

Sci Rep

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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...

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Section: Spindle Detectionmentioning

confidence: 95%

Section: Spindle Detectionmentioning

confidence: 99%

mentioning

confidence: 96%

mentioning

confidence: 99%

mentioning

confidence: 99%

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

Iotchev

Szabó

Kis

et al. 2020

Sci Rep

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Sleep-physiological correlates of brachycephaly in dogs

Iotchev,

Bognár,

Tóth

et al. 2023

Brain Struct Funct

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The shape of the cranium is one of the most notable physical changes induced in domestic dogs through selective breeding and is measured using the cephalic index (CI). High CI (a ratio of skull width to skull length > 60) is characterized by a short muzzle and flat face and is referred to as brachycephaly. Brachycephalic dogs display some potentially harmful changes in neuroanatomy, and there are implications for differences in behavior, as well. The path from anatomy to cognition, however, has not been charted in its entirety. Here, we report that sleep-physiological markers of white-matter loss (high delta power, low frontal spindle frequency, i.e., spindle waves/s), along with a spectral profile for REM (low beta, high delta) associated with low intelligence in humans, are each linked to higher CI values in the dog. Additionally, brachycephalic subjects spent more time sleeping, suggesting that the sleep apnea these breeds usually suffer from increases daytime sleepiness. Within sleep, more time was spent in the REM sleep stage than in non-REM, while REM duration was correlated positively with the number of REM episodes across dogs. It is currently not clear if the patterns of sleep and sleep-stage duration are mainly caused by sleep-impairing troubles in breathing and thermoregulation, present a juvenile-like sleeping profile, or are caused by neuro-psychological conditions secondary to the effects of brachycephaly, e.g., frequent REM episodes are known to appear in human patients with depression. While future studies should more directly address the interplay of anatomy, physiology, and behavior within a single experiment, this represents the first description of how the dynamics of the canine brain covary with CI, as measured in resting companion dogs using a non-invasive sleep EEG methodology. The observations suggest that the neuroanatomical changes accompanying brachycephaly alter neural systems in a way that can be captured in the sleep EEG, thus supporting the utility of the latter in the study of canine brain health and function.

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Age-related effects on a hierarchical structure of canine cognition

Bognár,

Turcsán,

Faragó

et al. 2024

GeroScience

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The current study investigates whether there are statistically independent age-related influences on the canine cognitive structure and how individual factors moderate cognitive aging on both cross-sectional and longitudinal samples. A battery of seven tasks was administered to 129 pet dogs, on which exploratory and confirmatory factor analyses were employed to unveil the correlational structure underlying individual differences in cognitive performance. The best-fitting model featured a hierarchical structure with two first-order cognitive domains (individual problem solving, learning) and a second-order common factor. These higher order factors exhibited consistency over a period of at least 2.5 years. External validation linked the common factor positively to discrimination and reversal learning performance, exploration, neophilia, activity/excitability, and training level while negatively to cognitive dysfunction symptoms, suggesting that it is a good candidate for a general cognitive factor (canine g). Structural equation models identified three distinct age-related influences, operating on associative learning, on memory, and on canine g. Health status moderated the negative age-canine g relationship, with a stronger association observed in dogs with poorer health status, and no relationship for dogs in good health. On a longitudinal sample (N = 99), we showed that the direction and magnitude of change in canine g over up to 3 years is affected by various interactions between the dogs’ age, communication score, baseline performance, and time elapsed since the baseline measurement. These findings underscore the presence of a general cognitive factor in dogs and reveal intriguing parallels between human and canine aging, affirming the translational value of dogs in cognition and aging research.

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Age-related differences and sexual dimorphism in canine sleep spindles

Cited by 31 publications

References 67 publications

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

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

Sleep-physiological correlates of brachycephaly in dogs

Age-related effects on a hierarchical structure of canine cognition

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