Accumulating evidence from electrocorticogram (ECoG) recordings and imaging challenge traditional views of brain oscillations as spatially stationary periodic sources. Understanding the spatio-temporal dynamics of cortical activity requires novel measurement and analysis methodologies. We recorded broadband local field potential (LFP) across the whole neocortex in freely behaving rats using high-density flexible surface arrays using active transistors. 3D tracking and spatio-spectral analysis of recordings over long sessions enabled automatic and accurate brain and behavioral states segmentation. Sleep spindles were identified as transient and spatially localized oscillatory bursts with single cycles exhibiting complex and often spiraling spatio-temporal structure. To characterize the diverse spatio-spectral dynamics in the spindle band, we decomposed the power spectrograms across channels and frequency bins by factor analysis. A principal-component analysis step is followed by rotation of the eigenvectors to maximize the simplicity criterion, that is, finding a set of maximally sparse and orthogonal loadings in space and frequency. Spatio-spectral structure of the factor loadings reflects oscillatory modes with diverse spatio-spectral characteristics and the respective factor score activation dynamics display transient bouts corresponding to waxing and waning oscillations, providing a lower dimensional description of the spindle power dynamics, resulting in matching factors across animals with similar spatio-spectral characteristics and comparable sleep spindles duration distributions. After characterizing the local generators of sleep spindles, we evaluate whether they are differentially coupled to slower field potential dynamics and how their activation rates change during slow-wave sleep and intermediate sleep. Inspection of the spindle band power dynamics reveals topographically structured patterns that presumably reflect the entrainment of various cortico-thalamic networks at the spindle band frequency, which possibly contribute differentially to consolidation of heterogeneous cortex-wide memory engrams, to test this we established modality-specific object-location memory tasks which in future combined with ECoG recordings may discover the role of sleep spindle motifs in targeted memory consolidation processes.