Heterogeneous Synaptic Homeostasis: A Novel Mechanism Boosting Information Propagation in Neural Circuitry

Abstract

Behavioral responses to auditory stimuli decrease from wakefulness to deep phases of sleep. This reduction in behavioral responses can be attributed to the diminished efficiency of neural communications within the cerebral cortex. Substantial experimental evidence underscores that the spatiotemporal spread of neural responses to external stimuli within the cerebral cortex is more extensive during wakefulness compared to deep sleep. However, the fundamental neural mechanisms driving this phenomenon remain unclear. One potential candidate is synaptic upscaling of cortical excitatory connections during wakefulness, aligning with the synaptic homeostasis hypothesis. Nonetheless, we argue that a uniform synaptic upscaling in a balanced configuration, without overexcitation or overinhibition, during wakefulness is insufficient to explain this observation. Instead, we propose a hypothesis suggesting that synaptic upscaling during wakefulness should be heterogeneous to account for the heightened propagation of neural responses within the cerebral cortex. Specifically, we propose that the upscaling of excitatory connections between distinct cortical areas (inter-excitatory connections) should exceed that within each cortical area (intraexcitatory connections). To explore this hypothesis, we utilized a computational model of coupled cortical columns. Our findings reveal that synaptic upscaling during wakefulness introduces a dynamic interplay between inter- and intra-excitatory connections. Synaptic upscaling of inter-excitatory connections enhances the propagation of information content and neural responses to external inputs, while the synaptic upscaling of intraexcitatory connections has a diminishing effect. Our computational results suggest that synaptic upscaling during wakefulness should be heterogeneous, favoring inter-excitatory connections over intra-excitatory connections. This heterogeneity is crucial for facilitating the propagation of information content and neural responses across distinct cortical areas during wakefulness compared to deep sleep.