Human sleep spindles track experimentally excited brain circuits

Abstract

Spindles are hallmark oscillations during non-rapid-eye-movement (NREM) sleep. Together with slow oscillations (SOs), they are thought to play a mechanistic role in the consolidation of learned information. The quantity and spatial distribution of spindles has been linked to brain activity during learning before sleep and to memory performance after sleep. If spindles are drawn to cortical areas excited through pre-sleep learning tasks, this begs the question whether the spatial distribution of spindles is flexible, and whether their regional expression can also be manipulated with experimental brain stimulation. We used excitatory transcranial direct current stimulation (tDCS) to stimulate the left and right motor cortex in a repeated-measures experimental design. After stimulation, we recorded high-density electroencephalography (EEG) during sleep to test how local stimulation modulated the regional expression of sleep spindles. Indeed, we show that excitatory tDCS of local cortical sites before sleep biases the expression of spindles to the excited locations during subsequent sleep. No effects of localised tDCS excitation were seen for SOs. These results demonstrate that the spatial topography of sleep spindles is neither hard-wired nor random, with spindles being flexibly directed to exogenously excited cortical circuits. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=108 SRC="FIGDIR/small/631687v2_ufig1.gif" ALT="Figure 1"> View larger version (21K): org.highwire.dtl.DTLVardef@fb33c1org.highwire.dtl.DTLVardef@2f291org.highwire.dtl.DTLVardef@1831f08org.highwire.dtl.DTLVardef@16a7f6a_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOGraphical AbstractC_FLOATNO C_FIG Statement of SignificanceSpindles are signatures of NREM sleep linked to memory consolidation, intelligence, and neurological disorders. Recent work shows the spatial distribution of spindles mirrors cortical activation patterns during learning. If spindles are preferentially expressed at cortical sites engaged during prior waking, the question arises whether spindles can be directed by inducing excitation exogenously with non-invasive brain stimulation. Here, we applied anodal-tDCS to either left or right motor areas before a nap. Indeed, we found that spindle (and not SO) rates are greater at cortical sites excited by tDCS. This result suggests the spatial distribution of spindles is flexible and is sensitive to experimental excitatory stimulation. This has implications for targeted rehabilitation of specific cortical areas and for developing sleep-based brain-computer interfaces.