Sleep-Dependent Potentiation in the Visual System Is at Odds with the Synaptic Homeostasis Hypothesis

Study Objectives: Two commentaries recently published in SLEEP came to very different conclusions regarding how data from a mouse model of sleep-dependent neural plasticity (orientation-specific response potentiation; OSRP) fit with the synaptic homeostasis hypothesis (SHY). To assess whether SHY offers an explanatory mechanism for OSRP, we present new data on how cortical neuron firing rates are modulated as a function of novel sensory experience and subsequent sleep in this model system. Methods: We carried out longitudinal extracellular recordings of single-neuron activity in the primary visual cortex across a period of novel visual experience and subsequent sleep or sleep deprivation. Spontaneous neuronal firing rates and visual responses were recorded from the same population of visual cortex neurons before control (blank screen) or novel (oriented grating) stimulus presentation, immediately after stimulus presentation, and after a period of subsequent ad lib sleep or sleep deprivation. Results: Firing rate responses to visual stimuli were unchanged across waking experience, regardless of whether a blank screen or an oriented grating stimulus was presented. Firing rate responses to stimuli of the presented stimulus orientation were selectively enhanced across post-stimulus sleep, but these changes were blocked by sleep deprivation. Neuronal firing increased significantly across bouts of post-stimulus rapid eye movement (REM) sleep and slow wave sleep (SWS), but not across bouts of wake. Conclusions: The current data suggest that following novel visual experience, potentiation of a subset of V1 synapses occurs across periods of sleep. This finding cannot be explained parsimoniously by SHY.