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.

Figure 1

All dogs first attended an adaptation session and polysomnographic data was collected for three hours. Subsequently the learning and control condition followed in random order, each including another three hours recording session. Illustrations by first author.

Figure 2

Example event the script marked as a spindle for the 9–16 Hz target band. Timepoint zero marks the centre of a detection and 7.5 seconds of the signal before and after are plotted on a scale from 40 to −40 µV for the raw trace (A) and filtered trace (B). A time-frequency plot (C) displays the change in frequency power for the segment shown in (A) and (B). The example is taken from the control condition (Maya, 6 year old Golden Retriever ♂).

Figure 3

Effects of Learning and Sex on spindle density in the learning condition. Detections in the 9–16 Hz range. (A) A scatter plot for the correlation of spindle density (spindles/minute) with learning gain (% increase in performance after sleep). (B) Scatter plot, with medians and standard errors of learning gain, comparing female and male dogs (N = 15, 7 ♀, P = 0.022). (C) Scatter plot, with medians and standard errors of spindle density in the learning condition, comparing female and male dogs, using an independent samples t-test (N = 15, 7 ♀, P = 0.001)

Figure 4

Differences in Density between conditions. Detections in the 9–16 Hz range. (A) Before-after plot of spindle density for the learning and control conditions, compared with a paired samples t-test (N = 15, P = 0.04). (B) Before-after plot of spindle density for the learning and control conditions, excluding dogs with more than 10 days between sessions, compared with a paired samples t-test (N = 11, P = 0.01).

Figure 5

Sex differences (excluding neutered dogs). Detections in the 9–16 Hz range. (A) Scatter plot, medians and standard errors of spindle density in the control condition, comparing female and male dogs, using an independent samples t-test (N = 10, 4 ♀, P = 0.03). (B) Scatter plot, medians and standard errors of spindle density in the learning condition, comparing female and male dogs, using an independent samples t-test (N = 10, 4 ♀, P = 0.003).

Figure 6

Slow and fast spindles. (A) A scatter plot for the correlation of slow spindle density (spindles/minute) with learning gain (% increase in performance after sleep). (B) Scatter plot, medians and standard errors of slow spindle density in the learning condition, comparing female and male dogs, using an independent samples t-test (N = 15, 7 ♀, N = 0.011). (C) Before-after plot of slow spindle density for the learning and control conditions, excluding dogs with more than 10 days between sessions, compared with a paired samples t-test (N = 11, P = 0.014). (D) Scatter plot, medians and standard errors of fast spindle density in the learning condition, comparing female and male dogs, using an independent samples t-test (N = 15, 7 ♀, P = 0.027). (E) A scatter plot showing the match between age (in years) and age values predicted by estimates obtained from the mean amplitude, mean frequency and mean density of fast spindles. Dogs without detections were excluded to not skew the estimation of amplitude and frequency (N = 12).