Cortically coordinated NREM thalamocortical oscillations play an essential, instructive role in visual system plasticity

Abstract

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....

Sleep as therapy in neurodevelopmental disorders

“…In non‐REM sleep, physiological slow‐sleep spindles (which reflect highly coherent thalamocortical activity) and slow‐wave sleep have both been associated with better general cognitive abilities and declarative learning in school‐age children. Both non‐REM sleep neural oscillation patterns may induce brain plasticity by facilitating transfer of information from thalamic nuclei to neurons in the cerebral cortex, inducing long‐lasting adaptive changes in their response to stimulation …”

Network resonance during slow-wave sleep facilitates memory consolidation through phase-coding

“…While the present study is focused on matching parameters of computational models to data from the hippocampus during fear memory consolidation, we believe that the mechanisms outlined here may be universally true. For example, sleep, and sleep-associated network oscillations, are required for consolidation of experience-dependent sensory plasticity in the visual cortex (28,32,33). Moreover, similar frequency-dependent changes in neuronal firing rates are also observed across periods of sleep in the visual cortex (5).…”

“…C57BL/6J mice implanted with bundles of CA1 stereotrodes either underwent CFC (placement into a novel environmental context, followed 2.5 min later by a 2-s, 0.75 mA foot shock; n = 5 mice), sham conditioning (placement in a novel context without foot shock; Sham; n = 3 mice), or CFC followed by 6 h of sleep deprivation (a manipulation known to disrupt fear memory consolidation [18,19,27]; SD; n = 5 mice) ( Figure 2 ). Spike data from individual neurons was discriminated offline using standard methods (consistent waveform shape and amplitude on the two stereotrode wires, relative cluster position of spike waveforms in principle component space, ISI ≥ 1 ms) (5,17,18,20,28). Only neurons that were stably recorded and reliably discriminated throughout the entire baseline and post-conditioning period were included in subsequent analyses of network dynamics.…”

Non-REM sleep facilitates consolidation of contextual fear memory through temporal coding among hippocampal neurons

“…While the present study is focused on varying parameters of computational models to predict data from the CA1 network during CFM consolidation, we believe that the mechanisms outlined here may be universally true. For example, sleep, and sleep-associated network oscillations, are required for consolidation of experience-dependent sensory plasticity in the visual cortex [18,33,35], and disruption of other hippocampal oscillations during sleep disrupts consolidation of other forms of memory [12]. Moreover, similar frequency-dependent changes in neuronal firing rates are also observed across periods of sleep in the visual cortex [7] and frontal cortex [6].…”

“…"replay") in the hippocampus during NREM, together with spike timing dependent plasticity (STDP), restructures network activity in a manner similar to that observed in brain circuits across periods of sleep. This suggests that sleep actively promotes memory consolidation by switching the network from rate-based to firing phase-based information encoding.Oscillatory patterning of neuronal firing during sleep has been implicated in promoting synaptic plasticity and memory storage [12][13][14][15][16][17][18][19]. Network oscillations present in brain circuits during sleep have been implicated in promoting STDP by precisely timing the firing between pairs of neurons [14,15].…”