Brain Advance Access published online on July 5, 2007
Brain, doi:10.1093/brain/awm146
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Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans
ss31Department of Neurology, National Institute of Psychiatry and Neurology, Budapest, Hungary, 2Department of Neuroendocrinology, University of Lübeck, Lübeck, Germany, 3National Institute of Neurosurgery, Budapest, Hungary and 4MR Research Centre, Semmelweis University, Budapest, Hungary
Correspondence to:
Zsófia Clemens, PhD, National Institute of Psychiatry and Neurology, Department of Neurology, H-1021 Budapest, Hüvösvölgyi út 116, Hungary E-mail: clemens{at}opni.hu
Ripples are high-frequency oscillation bursts in the mammalian hippocampus mainly present during Non-REM sleep. In rodents they occur in association with sharp waves and are grouped by the cortical slow oscillation such that, in parallel with sleep spindles, ripple activity is suppressed during the hyperpolarized down-state and enhanced during the depolarized up-state. The temporal coupling between slow oscillations, spindles and ripples has been suggested to serve a hippocampo-neocortical dialogue underlying memory consolidation during sleep. Here, we examined whether a similar coupling exists between these oscillatory phenomena in humans. In sleep recordings from seven epileptic patients, scalp-recorded slow oscillations and spindles as well as parahippocampal ripples recorded from foramen ovale electrodes were identified by automatic algorithms. Additionally, ripple and spindle root mean square activity was determined for relevant frequency bands. Ripple density was higher during Non-REM than REM sleep (P < 0.001). Ripple activity distinctly decreased time-locked to slow oscillation negative half-waves in the three patients without temporal structural alterations (P < 0.001), whereas in the four patients with severe mesiotemporal structural alterations this coupling was obscure. Generally, in the patients ripple activity was increased before spindle peaks and distinctly decreased after the peak (P < 0.001). Ripples were consistently associated with interictal spikes suggesting that spike–ripple complexes represent an epileptic transformation of sharp wave–ripple complexes in the epileptic hippocampus. Our findings are consistent with the notion of a hippocampo-to-neocortical information transfer during sleep that is linked to coordinate ripple and spindle activity, and that in the intact temporal lobe is synchronized to cortical slow oscillations.
Key Words: sleep; hippocampus; sharp wave–ripples; slow oscillation; epilepsy
Abbreviations: EOG, electrooculogram; EMG, electromyogram; FIR, finite impulse response; SPW, sharp wave
Received November 22, 2006. Revised May 10, 2007. Accepted May 31, 2007.
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