Thalamocortical and Intracortical Laminar Connectivity Determines Sleep Spindle Properties

Spindle oscillations are brief oscillatory activity during non-rapid eye movement (NREM) sleep. Spindle density and synchronization properties are different in MEG versus EEG recordings in humans and also vary with learning performance, suggesting spindle involvement in memory consolidation. Using computational models, we identified network mechanisms that may explain differences in spindle properties across cortical structures. First, we report that differences in spindle occurrence between MEG and EEG data may arise from the properties of the core vs. matrix thalamocortical systems. The matrix system, projecting superficially, has wider thalamocortical fanout compared to the core system, projecting to the middle layers, and requires the recruitment of a larger population of neurons to initiate a spindle. Our model demonstrates that this property is sufficient to explain lower spindle density and higher spatial synchrony of spindles in the superficial cortical layers, as observed in the EEG signal. In contrast, spindles in the core system occurred more frequently but less synchronously, as observed in the MEG recordings. Futhermore, consistent with human recordings, in the model, spindles occurred independently in the core system but matrix system spindles commonly co-occurred with core one. We found that the intracortical excitatory connections from layer III/IV to layer V promote spindle propagation from the core to the matrix system, leading to widespread spindle activity. Our study predicts that plasticity of the intra and inter cortical connectivity can potentially be a mechanism for increasing in spindle density as observed during learning. Author summary The density of sleep spindles has been shown to correlate with memory consolidation. Further, sleep spindles occur more often in human MEG than EEG. We developed thalamocortical network model that is capable of spontaneous generation of spindles across cortical layers and that captures the essential statistical features of spindles observed in experiments. We predict that differences in thalamo-cortical connectivity, known from anatomical studies, lead to the differences in the spindle properties between EEG and MEG as observed in human recordings. Further, we predict that the intracortical connectivity between cortical layers, a property influenced by sleep preceding learning, increases spindle density. Results from our study highlight the role of cortical and thalamic projections on the occurrence and properties of spindles.