Temporal association between sleep spindles and ripples in the human anterior and mediodorsal thalamus
European Journal of Neuroscience; Volume 59, Issue 4 p. 641-661; Special Issue Article; First published: 14 January 2024 (2024)
DOI: 10.1111/ejn.16240
Orsolya Szalárdy 1,2, Péter Simor 3,4, Péter Przemyslaw Ujma 1, Zsófia Jordán 5, László Halász 5, Loránd Erőss 5, Dániel Fabó 5, Róbert Bódizs 1
1 Institute of Behavioural Sciences, Semmelweis University, Budapest, Hungary
2 Institute of Cognitive Neuroscience and Psychology, Budapest, Hungary
3 Institute of Psychology, ELTE, Eötvös Loránd University, Budapest, Hungary
4 UR2NF, Neuropsychology and Functional Neuroimaging Research Unit at CRCN, Center for Research in Cognition and Neurosciences and UNI-ULB Neurosciences Institute, Université Libre de Bruxelles, Brussels, Belgium
5 National Institute of Mental Health, Neurology and Neurosurgery, Budapest, Hungary
ABSTRACT
Sleep spindles are major oscillatory components of Non-Rapid Eye Movement (NREM) sleep, reflecting hyperpolarization-rebound sequences of thalamocortical neurons. Reports suggest a link between sleep spindles and several forms of high-frequency oscillations which are considered as expressions of pathological off-line neural plasticity in the central nervous system. Here we investigated the relationship between thalamic sleep spindles and ripples in the anterior and mediodorsal nuclei (ANT and MD) of epilepsy patients. Whole-night LFP from the ANT and MD were co-registered with scalp EEG/polysomnography by using externalized leads in 15 epilepsy patients undergoing a Deep Brain Stimulation protocol. Slow (~12 Hz) and fast (~14 Hz) sleep spindles were present in the human ANT and MD and roughly, 20% of them were associated with ripples. Ripple-associated thalamic sleep spindles were characterized by longer duration and exceeded pure spindles in terms of spindle power as indicated by time-frequency analysis. Furthermore, ripple amplitude was modulated by the phase of sleep spindles within both thalamic nuclei. No signs of pathological processes were correlated with measures of ripple and spindle association, furthermore, the density of ripple-associated sleep spindles in the ANT showed a positive correlation with verbal comprehension. Our findings indicate the involvement of the human thalamus in coalescent spindle-ripple oscillations of NREM sleep.