Sleep Slow-Wave Activity Reveals Developmental Changes in Experience-Dependent Plasticity

Abstract

Experience-dependent plasticity, the ability of the brain to constantly adapt to an ever-changing environment, has been suggested to be highest during childhood and to decline thereafter. However, empirical evidence for this is rather scarce. Slow-wave activity (SWA; EEG activity of 1-4.5 Hz) during deep sleep can be used as a marker of experience-dependent plasticity. For example, performing a visuomotor adaptation task in adults increased SWA during subsequent sleep over a locally restricted region of the right parietal cortex, which is known to be involved in visuomotor adaptation. Here, we investigated whether local experience-dependent changes in SWA vary as a function of brain maturation. Three age groups (children, adolescents, and adults) participated in a high-density EEG study with two conditions (baseline and adaptation) of a visuomotor learning task. Compared with the baseline condition, sleep SWA was increased after visuomotor adaptation in a cluster of eight electrodes over the right parietal cortex. The local boost in SWA was highest in children. Baseline SWA in the parietal cluster and right parietal gray matter volume, which both indicate region-specific maturation, were significantly correlated with the local increase in SWA. Our findings indicate that processes of brain maturation favor experience-dependent plasticity and determine how sensitive a specific brain region is for learning experiences. Moreover, our data confirm that SWA is a highly sensitive tool to map maturational differences in experience-dependent plasticity.

Molecular Mechanisms of Sleep Homeostasis in Flies and Mammals

“…Several of the experiments discussed above controlled for the amount of movement used to perform the task, suggesting that changes in SWA are sensitive to neural plasticity above and beyond any effect of neuronal activity per se. Moreover, the extent of the SWA increase depends on the complexity of the task, and thus presumably on the extent of the plasticity that it triggers (Wilhelm et al 2014). There is also evidence that the changes in SWA that follow increased neuronal activity and plasticity do not simply reflect metabolic changes, because the SWA time course is longer than that of metabolic markers such as glucose and lactate (Vyazovskiy et al 2004;Rempe and Wisor 2014).…”

Sleep and anxiety in late childhood and early adolescence

“…In adolescence, there is a greater than 60% decrease in slow wave sleep and delta activity, with a sharp decline beginning roughly with the onset of puberty (between ages 9 and 11 years) and flattening out around the age of 17 [61–63]. In support of a maturational effect, Wilhelm et al recently showed that local changes in slow wave activity following experience-dependent learning were stronger in 8–11 years old youth, relative to 12–17 year old youth and adults[64++]. Notably, the only study of gist memory during sleep in youth (ages 8–11) showed greater gist-extraction in youth relative to adults[65].…”

The Yin and Yang of Sleep and Attention

“…Similarly, flies that are reared in more social environments or exposed to visual and tactile stimuli need to sleep more, as well as more deeply [57, 86-88], possibly because they are exposed to greater novelty. Interestingly, human attention disorders such as autism, schizophrenia and attention-deficit/hyperactivity disorder (ADHD) have also been associated with reduced or disrupted sleep [89-91], whereas periods of intense learning such as childhood and adolescence are associated with a greater need for sleep and a greater amount of slow-wave activity after learning [10, 92]. In summary, a number of studies suggest that sleep may be influenced by learning and attention in different species, supporting the view that sleep and attention may regulate each other bi-directionally.…”