Slow Wave Activity as Substrate of Homeostatic Regulation

Abstract

During the last 15–20 years, a new knowledge accumulated about NREM slow wave oscillations that have become the key issue of homeostatic regulation. A frequency-based classification of slow waves has been developed, differentiating between 0.1–1- and 1–4-Hz groups. The cortical <1-Hz slow activity during the so-called up states (surface-positive half wave), even ripple-like (50–200 Hz) fast activity, and down state (surface-negative half wave), an interruption of synaptic and neural activity, have been described. The alternation of these two microstates ensures a unique double working mode for the cortex, providing continuity for the contact and information processing with the environment during the up states even in deep sleep and providing a separation for trophotropic functions for further cognitive demands during the down states.

With progressive development of neuroimaging, source modeling studies on sleep slow waves by new neuroimaging tools have confirmed that the cortical areas are differentially involved in slow wave production and showed that sleep slow waves can be locally – mainly frontally – regulated. They are traveling along an anterior-posterior axis largely mediated by the so-called cingulate highway. Studies in this field emphasized that those areas with maximal involvement in slow waves’ production also show considerable overlap with the default network, paradoxically implicated in monitoring the external environment, and can be altered by sleep deprivation.

Ontogenetic studies revealed that the delta oscillation associated with rapid spindling is the agent of plastic changes of the cortex. Reactive (input-dependent) delta activity seems to be an essential element of plastic changes as early as during the neonatal development. Before the fetal brain might receive elaborated sensory inputs from the external word, spontaneous fetal movements provide sensory stimulation and drive delta-brush oscillation, contributing to the formation of cortical body maps.

The spectral power of sleep slow wave activity and the steepness of the slopes of sleep slow waves were shown to correlate positively with the gray matter volume of several cortical areas in children and adolescents between 8 and 19 years of age. When the production of cortical synapses is more efficient than their elimination (from birth until the prepubertal age), slow wave activity is high and increasing; while in adulthood, when the elimination of synapses exceeds their production, the amount of sleep slow wave activity decreases.

Discussing phylogenetic relations of slow wave activity during different vigilance states and state-dependent reactions to sensory inputs, we try to interpret some paradoxical observations on reptiles. We are proposing that the reason why reptiles are in a continuous NREM sleep like condition during behavioral waking state is the lack or underdevelopment of their cholinergic arousal system. Therefore, sensory stimulation elicits K-complex-like slow wave responses. In the waking state, reptiles apparently have sleep EEG and sleep-like EEG activity during behavioral activation. Our proposal incorporates an explanation for the lack of long-term homeostatic sleep regulation in reptiles, having at the same time short-term homeostatic slow wave supplementation in response to sensory stimulation.