EEG Transients in the Sigma Range During non-REM Sleep Predict Learning in Dogs

Abstract

Sleep spindles are phasic bursts of thalamo-cortical activity, visible in the cortex as transient oscillations in the sigma range (usually defined in humans as 12–14 or 9–16 Hz). They have been associated with sleep-dependent memory consolidation and sleep stability in humans and rodents. Occurrence, frequency, amplitude and duration of sleep spindles co-vary with age, sex and psychiatric conditions. Spindle analogue activity in dogs has been qualitatively described, but never quantified and related to function. In the present study we used an adjusted version of a detection method previously validated in children to test whether detections in the dogs show equivalent functional correlates as described in the human literature. We found that the density of EEG transients in the 9–16 Hz range during non-REM sleep relates to memory and is characterized by sexual dimorphism similarly as in humans. The number of transients/minute was larger in the learning condition and for female dogs, and correlated with the increase of performance during recall. It can be concluded that in dogs, automatic detections in the 9–16 Hz range, in particular the slow variant (<13 Hz), are functional analogues of human spindles.

Characterizing Sleep Spindles in Sheep

“…Finally, in order to be included, a filtered spindle needed to contain at least three positive peaks. We allowed our algorithm to detect spindles between 5 and 16 Hz because spindles in other animal models have been found at lower frequencies than those in humans (Contreras and Steriade, 1996;Iotchev et al, 2017). However, we found no evidence of a clear separation in spindle frequency bands (data not shown); therefore, in this article we have focused on spindles falling into the classical range of 10-16 Hz.…”

“…The apparent function of fast and slow spindles also varies. In dogs, only slow spindles (,13 Hz) predict learning ability (Iotchev et al, 2017), while in rats only fast spindles (.12 Hz) correlate with learning (Eschenko et al, 2006).…”

“…Sleep spindles are transient and distinctive patterns of brain activity that typically occur during non-rapid eye movement (NREM) sleep in humans. They have been documented in several other animal species, including mice (Kim et al, 2015), rats (Eschenko et al, 2006), dogs (Iotchev et al, 2017), cats (Contreras and Steriade, 1996), monkeys (Takeuchi et al, 2016), and ferrets (McCormick and Bal, 1997). Sleep spindles are considered to play a key role in memory consolidation and have been studied in relation to both learning ability and cognitive impairment (Clemens et al, 2005;Eschenko et al, 2006;Iotchev et al, 2017).…”

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

“…Day-to-day fluctuations in spindle occurrence and frequency may explain why difference score comparisons have mostly been avoided. Sources of such variation include the menstrual cycle [35][36][37][38] , and simple exposure to novel information, which increases spindle occurrence in humans [39][40][41] , rats 41,42 , and dogs 10 . It seems, therefore, that without controlling for hormonal levels and pre-sleep experience, comparing spindle activity and memory performance measured further away than a day from each other could be problematic.…”

“…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.…”