Local sleep spindles in the human thalamus

Abstract

Key points Sleep spindles have recently been shown to occur not only across multiple neocortical regions but also locally in restricted cortical areas. Here we show that local spindles are indeed present in the human posterior thalamus. Thalamic local spindles had lower spectral power than non‐local ones. While non‐local thalamic spindles had equal local and non‐local cortical counterparts, local thalamic spindles had significantly more local cortical counterparts (i.e. occurring in a single cortical site). The preferential association of local thalamic and cortical spindles supports the notion of thalamocortical loops functioning in a modular way. Abstract Sleep spindles are believed to subserve many sleep‐related functions, from memory consolidation to cortical development. Recent data using intracerebral recordings in humans have shown that they occur across multiple neocortical regions but may also be spatially restricted to specific brain areas (local spindles). The aim of this study was to characterize spindles at the level of the human posterior thalamus, with the hypothesis that, besides the global thalamic spindling activity usually observed, local spindles could also be present in the thalamus. Using intracranial, time‐frequency EEG recordings in 17 epileptic patients, we assessed the distribution of thalamic spindles during natural sleep stages N2 and N3 in six thalamic nuclei. Local spindles (i.e. spindles present in a single pair of recording contacts) were observed in all the thalamic regions explored, and compared with non‐local spindles in terms of intrinsic properties and cortical counterparts. Thalamic local and non‐local spindles did not differ in density, frequency or duration, but local spindles had lower spectral power than non‐local ones. Each thalamic spindle had a cortical counterpart. While non‐local thalamic spindles had equal cortical local and non‐local counterparts, local thalamic spindles had significantly more local cortical counterparts (i.e. occurring in a single cortical site). The preferential association of local thalamic and cortical spindles supports the notion of thalamocortical loops functioning in a modular way.

Focal Sleep Spindle Deficits Reveal Focal Thalamocortical Dysfunction and Predict Cognitive Deficits in Sleep Activated Developmental Epilepsy

“…Although thalamocortical circuit dysfunction has previously been implicated in the pathophysiology of generalized seizures in absence epilepsy (Williams, 1953;Beenhakker and Huguenard, 2009;Maheshwari and Noebels, 2014;Fogerson and Huguenard, 2016), our observation of a focal spindle deficit in CECTS reveals that thalamocortical circuit can be focally disrupted in epilepsy. Consistent with this, prior work has demonstrated that distinct thalamocortical assemblages generate focal spindles (Andersen et al, 1967;Bastuji et al, 2020), and these distinct circuits can promote focal abnormalities (Fogerson and Huguenard, 2016;Clemente-Perez et al, 2017). In particular, sensorimotor thalamocortical circuits promote spatially distinct spindle populations (Nishida and Walker, 2007;Fogerson and Huguenard, 2016), and these sensorimotor spindles have been mechanistically tied to focal seizures in mouse models (Clemente-Perez et al, 2017).…”

Sleep spindles comprise a subset of a broader class of electroencephalogram events

“…The simplest possibility is that TFσ peaks are generated by the exact same mechanism as spindles and that any differences are purely a consequence of selection bias. Spindle power measured at the scalp can vary with the degree with which a spindle is local or global [ 50 , 51 ]. Alternatively, high-powered spindles emanating from cortical locations more distant from the recording electrode might appear to be weaker when propagated via volume conduction [ 52 , 53 ].…”

Sleep spindles, ripples, and interictal epileptiform discharges in the human anterior and mediodorsal thalamus

“…In contrast, IEDs in the human thalamus, such as in the ANT LFP records were observed and suggested the involvement of ANT in the propagation of epileptic activity and to contribute to the epileptic network (Hodaie et al, 2002; Sweeney-Reed et al, 2016). In several former studies, sleep spindles were recorded from the human thalamic nuclei, including the ANT and the posterior thalamus/medial pulvinar nucleus of epilepsy patients undergoing DBS or invasive presurgical neurophysiological investigation (Bastuji et al, 2020; Mak-Mccully et al, 2017; Tsai et al, 2010). Here we investigated the association between thalamic sleep spindles, interictal epileptiform discharges, ripples, and their associations with intellectual ability within two higher-order thalamic nuclei in human subjects, the ANT and the MD.…”