Aton SJ, Suresh A, Broussard C, Frank MG. Sleep promotes cortical response potentiation following visual experience.

Oscillations in the hippocampal network during sleep are proposed to play a role in memory storage by patterning neuronal ensemble activity. Here we show that following single-trial fear learning, sleep deprivation (which impairs memory consolidation) disrupts coherent firing rhythms in hippocampal area CA1. State-targeted optogenetic inhibition of CA1 parvalbumin-expressing (PV+) interneurons during postlearning NREM sleep, but not REM sleep or wake, disrupts contextual fear memory (CFM) consolidation in a manner similar to sleep deprivation. NREM-targeted inhibition disrupts CA1 network oscillations which predict successful memory storage. Rhythmic optogenetic activation of PV+ interneurons following learning generates CA1 oscillations with coherent principal neuron firing. This patterning of CA1 activity rescues CFM consolidation in sleep-deprived mice. Critically, behavioral and optogenetic manipulations that disrupt CFM also disrupt learning-induced stabilization of CA1 ensembles’ communication patterns in the hours following learning. Conversely, manipulations that promote CFM also promote long-term stability of CA1 communication patterns. We conclude that sleep promotes memory consolidation by generating coherent rhythms of CA1 network activity, which provide consistent communication patterns within neuronal ensembles. Most importantly, we show that this rhythmic patterning of activity is sufficient to promote long-term memory storage in the absence of sleep.

Ocular dominance plasticity in the developing primary visual cortex is initiated by monocular deprivation (MD) and consolidated during subsequent sleep. To clarify how visual experience and sleep affect neuronal activity and plasticity, we continuously recorded extragranular visual cortex fast-spiking (FS) interneurons and putative principal (i.e., excitatory) neurons in freely behaving cats across periods of waking MD and post-MD sleep. Consistent with previous reports in mice, MD induces two related changes in FS interneurons: a response shift in favor of the closed eye and depression of firing. Spike-timing-dependent depression of open-eye-biased principal neuron inputs to FS interneurons may mediate these effects. During post-MD nonrapid eye movement sleep, principal neuron firing increases and becomes more phase-locked to slow wave and spindle oscillations. Ocular dominance (OD) shifts in favor of open-eye stimulation-evident only after post-MD sleep -are proportional to MD-induced changes in FS interneuron activity and to subsequent sleep-associated changes in principal neuron activity. OD shifts are greatest in principal neurons that fire 40-300 ms after neighboring FS interneurons during post-MD slow waves. Based on these data, we propose that MD-induced changes in FS interneurons play an instructive role in ocular dominance plasticity, causing disinhibition among open-eye-biased principal neurons, which drive plasticity throughout the visual cortex during subsequent sleep.period shifts neuronal responses in primary visual cortex in favor of open-eye stimulation. Sleep is essential for consolidating ocular dominance plasticity (ODP) in cat visual cortex (1, 2). Specifically, post-MD sleep is required to potentiate open-eye responses in cortical neurons-a process mediated via intracellular pathways involved in long-term potentiation of glutamatergic synapses (1, 3). However, the changes in network activity (during waking experience and subsequent sleep) that mediate ODP remain unknown.One long-standing hypothesis is that ODP is gated by the balance of excitation and inhibition in the visual cortex during the critical period. This idea is supported by findings that ODP is enhanced either by increasing GABAergic neurotransmission before the critical period (4) or by reducing GABA signaling after the critical period (5-8). It has been suggested that, during the critical period, MD itself alters the balance of excitation and feedback inhibition within the visual cortex by depressing the activity of fast-spiking (FS) interneurons (9, 10). In support of this idea, ODP is first detectable in the extragranular cortical layers [i.e., 2/3, 5, and 6 (11)], where depression of FS interneuron activity has been reported after brief MD. These layers are characterized by abundant reciprocal intralaminar connections between FS interneurons and pyramidal neurons (12, 13). In contrast, in layer 4, where ODP is initially weak or absent (11), connections between FS interneurons and pyramidal neurons can be strengthened by MD ...

Two long-standing questions in neuroscience are how sleep promotes brain plasticity and why some forms of plasticity occur preferentially during sleep vs. wake. Establishing causal relationships between specific features of sleep (e.g., network oscillations) and sleep-dependent plasticity has been difficult. Here we demonstrate that presentation of a novel visual stimulus (a single oriented grating) causes immediate, instructive changes in the firing of mouse lateral geniculate nucleus (LGN) neurons, leading to increased firing-rate responses to the presented stimulus orientation (relative to other orientations). However, stimulus presentation alone does not affect primary visual cortex (V1) neurons, which show response changes only after a period of subsequent sleep. During poststimulus nonrapid eye movement (NREM) sleep, LGN neuron overall spike-field coherence (SFC) with V1 delta (0.5-4 Hz) and spindle (7-15 Hz) oscillations increased, with neurons most responsive to the presented stimulus showing greater SFC. To test whether coherent communication between LGN and V1 was essential for cortical plasticity, we first tested the role of layer 6 corticothalamic (CT) V1 neurons in coherent firing within the LGN-V1 network. We found that rhythmic optogenetic activation of CT V1 neurons dramatically induced coherent firing in LGN neurons and, to a lesser extent, in V1 neurons in the other cortical layers. Optogenetic interference with CT feedback to LGN during poststimulus NREM sleep (but not REM or wake) disrupts coherence between LGN and V1 and also blocks sleep-dependent response changes in V1. We conclude that NREM oscillations relay information regarding prior sensory experience between the thalamus and cortex to promote cortical plasticity. (5), and electrophysiological (2, 6-8) evidence supports the idea that following novel sensory experiences, sleep can promote cortical plasticity. The sleep-dependent mechanisms driving these changes have remained elusive. Sleep-associated changes in network activity (1, 6, 7, 9, 10), neuromodulator tone (11), transcription (4), translation (4), and protein phosphorylation (2, 3) have all been correlated with cortical plasticity following novel experiences (12). In recent years, neuroscientists have speculated that the high-amplitude, low-frequency thalamocortical oscillations that characterize nonrapid eye movement (NREM) sleep play a critical role in promoting sensory cortical plasticity and learning (12). While it has been hypothesized that such NREM oscillations promote general synaptic "downscaling" (13), converging data suggest that they could instead promote synaptic strengthening (5-7, 9). While rhythmic stimulation of the cortex at frequencies meant to mimic NREM oscillations (1-2 Hz) is sufficient to promote cortical plasticity and learning (9, 10), it is unclear whether naturally occurring oscillations are necessary for sleep-dependent processes. Another critical question is whether NREM oscillations play an instructive role in experience-initiated plasticity-i.e....

Recent studies suggest that sleep differentially alters the activity of cortical neurons based on firing rates during preceding wake—increasing the firing rates of sparsely firing neurons and decreasing those of faster firing neurons. Because sparsely firing cortical neurons may play a specialized role in sensory processing, sleep could facilitate sensory function via selective actions on sparsely firing neurons. To test this hypothesis, we analyzed longitudinal electrophysiological recordings of primary visual cortex (V1) neurons across a novel visual experience which induces V1 plasticity (or a control experience which does not), and a period of subsequent ad lib sleep or partial sleep deprivation. We find that across a day of ad lib sleep, spontaneous and visually-evoked firing rates are selectively augmented in sparsely firing V1 neurons. These sparsely firing neurons are more highly visually responsive, and show greater orientation selectivity than their high firing rate neighbors. They also tend to be “soloists” instead of “choristers”—showing relatively weak coupling of firing to V1 population activity. These population-specific changes in firing rate are blocked by sleep disruption either early or late in the day, and appear to be brought about by increases in neuronal firing rates across bouts of rapid eye movement (REM) sleep. Following a patterned visual experience that induces orientation-selective response potentiation (OSRP) in V1, sparsely firing and weakly population-coupled neurons show the highest level of sleep-dependent response plasticity. Across a day of ad lib sleep, population coupling strength increases selectively for sparsely firing neurons—this effect is also disrupted by sleep deprivation. Together, these data suggest that sleep may optimize sensory function by augmenting the functional connectivity and firing rate of highly responsive and stimulus-selective cortical neurons, while simultaneously reducing noise in the network by decreasing the activity of less selective, faster-firing neurons.