Top-down cortical input during NREM sleep consolidates perceptual memory

Abstract

During tactile perception, long-range intracortical top-down axonal projections are essential for processing sensory information. Whether these projections regulate sleep-dependent long-term memory consolidation is unknown. We altered top-down inputs from higher-order cortex to sensory cortex during sleep and examined the consolidation of memories acquired earlier during awake texture perception. Mice learned novel textures and consolidated them during sleep. Within the first hour of non-rapid eye movement (NREM) sleep, optogenetic inhibition of top-down projecting axons from secondary motor cortex (M2) to primary somatosensory cortex (S1) impaired sleep-dependent reactivation of S1 neurons and memory consolidation. In NREM sleep and sleep-deprivation states, closed-loop asynchronous or synchronous M2-S1 coactivation, respectively, reduced or prolonged memory retention. Top-down cortical information flow in NREM sleep is thus required for perceptual memory consolidation.

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

“…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)(8)(9)(10)(11)(12)(13)(14)(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.…”

“…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).…”

Cycle-Triggered Cortical Stimulation during Slow Wave Sleep Facilitates Learning a BMI Task: A Case Report in a Non-Human Primate

“…Our results show that delta-coupled stimulation in phase with SWS up-states facilitated learning of a BMI task over a second competitive one. Besides being a local phenomenon (Ghilardi et al, 2000; Huber et al, 2004, 2006), SWS has been described as a global phenomenon (i.e., occurring in phase across most brain areas), which allows concurrent reactivation of the newly encoded traces in different structures, including the hippocampus and neocortex, thereby serving to potentiate the cortico-cortical connections underlying stored representations (Logothetis et al, 2012; Miyamoto et al, 2016). Slow oscillations generate an important functional reorganization of cortical network that supports the consolidation of memories (Sirota et al, 2003; Sirota and Buzsáki, 2005; Genzel et al, 2014).…”

Causal Role of Neural Signals Transmitted From the Frontal Eye Field to the Superior Colliculus in Saccade Generation

“…Photo-stimulation of the ChR2 expressed on axon terminals induces a synaptic response to evoke signal transmission connecting the two regions. This methodology has brought substantial success in modulating behaviors in rodents (Stuber et al, 2011; Tye et al, 2011; Stamatakis and Stuber, 2012; Warden et al, 2012; Ahmari et al, 2013; Miyamoto et al, 2016), and has advanced our understanding of the roles of particular neural pathways in behaviors. However, the use of this methodology has greatly been restricted to small animals, and its application to primates which have much larger brains than rodents has so far been limited.…”

“…Such optogenetic methodology has brought substantial success in modulating behaviors in rodents (Stuber et al, 2011; Tye et al, 2011; Stamatakis and Stuber, 2012; Warden et al, 2012; Ahmari et al, 2013; Miyamoto et al, 2016), and has advanced our understanding of the roles of particular neural circuits in behaviors. After reviewing the electrophysiological and pharmacological studies, we highlight a recent attempt of our own that has applied an optogenetic approach to stimulate the neural pathway from the FEF to the SC in macaque monkeys.…”