Sleep-Dependent Sensory Gating and Synaptic Priming Mechanisms

The synaptic homeostasis hypothesis (SHY), a leading hypothesis on sleep, proposes that sensorial input during wakefulness increases synaptic potentiation, diminishing available neuroplastic capacity for future learning and so requiring renormalization during sleep. Faced with ongoing novelty, the organizational resources of brain synapses are posited to regularly operate within physical ranges that encounter upper limits. Sleep, accordingly, is considered vital not merely for the restoration of depleted resources but for preservation of the ability to optimally utilize sensorial information and neuroplastic resources. Based on this understanding, several structural and functional outcomes can be predicted, which have been supported by empirical observation. First, the acquisition of neuroplastic change is confined to periods of waking, when responsivity is maximal, rather than during sleep, when neural activity is at least partly disconnected from the external world. Second, such change occurs globally; that is, at a minimum it is found in all brain domains having sensorial input and likely also affects downstream targeted destinations. Third, renormalization occurs cyclically, a conclusion that is implicit in the first two consequences of this hypothesis, allowing both maximal learning and maximal recovery for learning to occur. Fourth, renormalization subserves behaviorally significant learning functions, those of maintaining neuroplastic and behavioral capacities. Extant studies supporting these predictions reveal the presence of sleep induced mechanisms that operate throughout the cortical and much of the subcortical domains. A key mechanism engaging renormalization, notably, is the slow oscillation, whose synchronized activity pervades the cortex and activates down selection according to spike timing dependent plasticity rules. Thalamic gating of afferent input appears to originate within thalamic nuclei, affecting the initiation of slow wave up states and frequency of the slow wave oscillation. Importantly, while the SHY hypothesis may be interpreted as a non-specific, globally directed process for renormalization of synapses that experience substantial neuroplastic change; that is, subserving a chiefly homeostatic role, other studies indicate that renormalization entails the targeted removal of behaviorally irrelevant or minimally relevant, learned information or responses that might otherwise distort learned behaviors. Hence, sleep appears to optimize interactive responsivity bimodally by strengthening a small subset of neuroplastically altered circuits and pruning away a much larger subset of non-specifically modulated networks; that is, learning and forgetting are biologically regulated functions enabling optimal adaptability to an everchanging environment