NeuroImage Volume 226, 117587 (2021) (Open Access Article)
Péter P. Ujmaa,b, Boglárka Hajnalb,c, Róbert Bódizsa,b, Ferenc Gombosd,e, Loránd Erőssb, Lucia Wittnerb,f,j, Eric Halgreng, Sydney S. Cashh,i, István Ulbertb,f,j, Dániel Fabób
a Institute of Behavioural Sciences, Semmelweis University, 1089 Budapest, Hungary
b Epilepsy Centrum, Dept. of Neurology, National Institute of Clinical Neurosciences, 1145 Budapest, Hungary
c School of P.h.D. studies, Semmelweis University, 1085 Budapest, Hungary
d Department of General Psychology, Pázmány Péter Catholic University, 1088 Budapest, Hungary
e MTA-PPKE Adolescent Development Research Group, Hungarian Academy of Sciences, 1088 Budapest, Hungary
f Institute of Cognitive Neuroscience and Psychology, Research Centre for Natural Sciences, Eötvös Loránd Research Network 1117 Budapest, Hungary
g Departments of Radiology and Neurosciences, University of California, 92093 San Diego CA, USA
h Center for Neurotechnology and Neurorecovery (CNTR), Department of Neurology, Massachusetts General Hospital, 02114 Boston, MA, USA
i Department of Neurology, Harvard Medical School, Boston, 02115 MA, USA
j Faculty of Information Technology and Bionics, Pázmány Péter Catholic University, 1088 Budapest, Hungary
Abstract
Sleep spindles are functionally important NREM sleep EEG oscillations which are generated in thalamocortical, corticothalamic and possibly cortico-cortical circuits. Previous hypotheses suggested that slow and fast spindles or spindles with various spatial extent may be generated in different circuits with various cortical laminar innervation patterns. We used NREM sleep EEG data recorded from four human epileptic patients undergoing presurgical electrophysiological monitoring with subdural electrocorticographic grids (ECoG) and implanted laminar microelectrodes penetrating the cortex (IME). The position of IMEs within cortical layers was confirmed using postsurgical histological reconstructions. Many spindles detected on the IME occurred only in one layer and were absent from the ECoG, but with increasing amplitude simultaneous detection in other layers and on the ECoG became more likely. ECoG spindles were in contrast usually accompanied by IME spindles. Neither IME nor ECoG spindle cortical profiles were strongly associated with sleep spindle frequency or globality. Multiple-unit and single-unit activity during spindles, however, was heterogeneous across spindle types, but also across layers and patients. Our results indicate that extremely local spindles may occur in any cortical layer, but co-occurrence at other locations becomes likelier with increasing amplitude and the relatively large spindles detected on ECoG channels have a stereotypical laminar profile. We found no compelling evidence that different spindle types are associated with different laminar profiles, suggesting that they are generated in cortical and thalamic circuits with similar cortical innervation patterns. Local neuronal activity is a stronger candidate mechanism for driving functional differences between spindles subtypes.