Abstract
During sleep, the thalamus generates a characteristic pattern of transient, 11-15 Hz sleep spindle oscillations, which synchronize the cortex through large-scale thalamocortical loops. Spindles have been increasingly demonstrated to be critical for sleep-dependent consolidation of memory, but the specific neural mechanism for this process remains unclear. We show here that cortical spindles are spatiotemporally organized into circular wave-like patterns, organizing neuronal activity over tens of milliseconds, within the timescale for storing memories in large-scale networks across the cortex via spike-time dependent plasticity. These circular patterns repeat over hours of sleep with millisecond temporal precision, allowing reinforcement of the activity patterns through hundreds of reverberations. These results provide a novel mechanistic account for how global sleep oscillations and synaptic plasticity could strengthen networks distributed across the cortex to store coherent and integrated memories.
Highlights
Memories are stored in distributed networks across the cortex
In the two-stage model of memory consolidation (McClelland et al, 1995; Rasch and Born, 2007), memories are integrated in the hippocampus and linked in the neocortex for long-term storage, where information represented in visual, auditory, somatosensory, or cognitive regions must be bound into a coherent whole (Wheeler et al, 2000; Horner et al, 2015)
It is well established that sleep oscillations actively contribute to this process: during stage 2 sleep spindles, the thalamus generates a rhythmic activity pattern that becomes widespread through large-scale thalamocortical loops (Contreras et al, 1996), and spindles are critical to sleep-dependent memory consolidation (Gais et al, 2002; Mednick et al, 2013)
Summary
Memories are stored in distributed networks across the cortex. In the two-stage model of memory consolidation (McClelland et al, 1995; Rasch and Born, 2007), memories are integrated in the hippocampus and linked in the neocortex for long-term storage, where information represented in visual, auditory, somatosensory, or cognitive regions must be bound into a coherent whole (Wheeler et al, 2000; Horner et al, 2015). These patterns most likely represent the characteristic spatiotemporal organization of the ’global’ spindles observed in Andrillon et al (Andrillon et al, 2011) (!40% involvement, cf their Figure 5C), with more localized patterns left unclassified by our detection approach (Figure 1—figure supplements 9 and 12) These global patterns are likely established through widespread thalamocortical loops, placing the cortex into a state of large-scale coherence (Contreras et al, 1996), shaped into rotating and expanding waves through corticocortical white matter connections with axonal conduction speeds consistent with the observed propagation speeds (Figure 1C). These results provide insight into how distributed information stored across cortical regions may be bound into a coherent, integrated, but specific memory through spike-time dependent synaptic plasticity
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