The human thalamus orchestrates neocortical oscillations during NREM sleep

Schreiner, Thomas; Kaufmann, Elisabeth; Noachtar, Soheyl; Mehrkens, Jan-Hinnerk; Staudigl, Tobias

doi:10.1038/s41467-022-32840-w

Cited by 40 publications

(31 citation statements)

References 77 publications

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“…As such, we combined recordings from anterior and centromedian nuclei. Recent work (Schreiner et al, 2022) has suggested that there may be differences in which area receives slow oscillations from the cortex (centromedian) and which area generates slow oscillations (anterior nucleus). In Schreiner et al (2022) only 30% of neocortical slow oscillations were connected to anterior thalamic slow oscillations, suggesting most neocortical slow oscillations may still be cortically generated.…”

Section: Discussionmentioning

confidence: 99%

“…For epileptic spike and spindle detections we evaluated three voltage time series from each subject: 1) Adjacent thalamic depth electrode contacts with the highest amplitude signal in a bipolar reference; 2) Adjacent cortical depth electrode contacts in the clinically determined seizure onset zone in a bipolar reference; 3) Scalp EEG in a bipolar reference CZ-PZ. To detect slow oscillations, we analyzed the scalp CZ contact using a far-field non-cephalic reference placed over the second cortical spinous process (Schreiner et al, 2022;Staresina et al, 2015).…”

Section: Eeg Data Collection Pre-processing and Channel Selectionmentioning

confidence: 99%

“…Sleep spindles originate in the thalamus and propagate to the cortex and occur with an approximate period of 2-5 s, dictated by an after-depolarization spindle refractory period (Bal & McCormick, 1996;Fernandez & Lüthi, 2020). Spindles are frequently nested in the up-state of slow oscillations -0.5-2 Hz oscillations - (Mak-McCully et al, 2017;Schreiner et al, 2022;Steriade et al, 1993) and, critically, may coordinate hippocampal ripples to support memory consolidation (Latchoumane et al, 2017;Staresina et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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Human thalamic recordings reveal that epileptic spikes block sleep spindle production during non-rapid eye movement sleep

Wodeyar

Chinappen

Mylonas

et al. 2023

Preprint

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In severe epileptic encephalopathies, epileptic activity contributes to progressive cognitive dysfunction. Several epileptic encephalopathies share the trait of spike-wave activation during non-rapid eye movement sleep (EE-SWAS), a state dominated by sleep oscillations known to coordinate offline memory consolidation. How epileptic activity impacts these thalamocortical sleep oscillations has not been directly observed in humans. Using a unique dataset of simultaneous human thalamic and cortical recordings in subjects with and without EE-SWAS, we reconcile prior conflicting observations about how epileptic spikes coordinate with sleep oscillations and provide direct evidence for epileptic spike interference of sleep spindle production. We find that slow oscillations facilitate both epileptic spikes and sleep spindles during stage 2 sleep (N2) at different phases of the slow oscillation. We show that sleep activated cortical epileptic spikes propagate to the thalamus (thalamic spike rate is increased after a cortical spike, p~0). Thalamic spikes increase the spindle refractory period (p<1.5e-21). In patients with EE-SWAS, the abundance of thalamic spikes result in downregulation of spindles for 30 seconds after each thalamic spike (p=3.4e-11) and decreased overall spindle rate across N2 (p=2e-7). These direct human thalamocortical observations identify a novel mechanism through which epileptiform spikes could impact cognitive function, wherein sleep-activated epileptic spikes inhibit thalamic sleep spindles in epileptic encephalopathy.

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Section: Discussionmentioning

confidence: 99%

Section: Eeg Data Collection Pre-processing and Channel Selectionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Human thalamic recordings reveal that epileptic spikes block sleep spindle production during non-rapid eye movement sleep

Wodeyar

Chinappen

Mylonas

et al. 2023

Preprint

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“…Indeed, coordinating influences of breathing on brain rhythms have been demonstrated in several brain areas linked to memory processes, including not only the hippocampus 17,[36][37][38] , but also thalamus 39 and prefrontal cortex 22,40 . Notably, these three regions also represent key structures for sleep-related memory consolidation, giving rise to ripples, sleep spindles and SOs, respectively [41][42][43] . In fact, recent work in rodents has demonstrated that respiration modulates the coordination of hippocampal sharp-wave ripples and cortical down/upstate transitions during NREM sleep 39 , while theta and gamma and their interplay during REM sleep are likewise impacted by breathing 44,45 .…”

Section: Discussionmentioning

confidence: 99%

Respiration shapes sleep-oscillations and memory reactivation in humans

Schreiner

Petzka

Staudigl

et al. 2023

Preprint

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The beneficial effect of sleep on memory consolidation relies on the precise interplay of slow oscillations (SOs) and spindles. However, whether these rhythms are orchestrated by an underlying pacemaker has remained elusive. Here, we tested whether respiration, which has been shown to impact brain rhythms and cognition during wake, shapes memory reactivation by modulating sleep-related oscillations and their interplay in humans. We recorded scalp EEG and respiration throughout an experiment in which participants acquired associative memories before taking a nap. Our results reveal that respiration strongly modulates the emergence of sleep oscillations. Specifically, SOs, spindles as well as their interplay (i.e., coupled SO_spindle complexes) systematically increase towards inhalation peaks. Moreover, the strength of respiration-SO_spindle coupling is linked to the extent of memory reactivation during SO_spindles. Our results identify respiration as a potential pacemaker for memory consolidation in humans and highlight the critical role of brain-body interactions during sleep.

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“…In the ventral part, the reticular nucleus' inhibitory neurons establish connections both with each other and with neurons in the dorsal nuclei, to regulate and foster communication inside the thalamus [8,9]. The interactions between the dorsal and ventral parts of the thalamus allow for the generation of sustainable oscillations of neural activity, such as delta oscillations, sleep spindles, and slow waves, that may propagate to the cortex and influence its dynamics [10][11][12][13][14][15]. The intralaminar part is involved in the RAS [16] delivering cholinergic and monoaminergic neurotransmission diffusely to the cortex and controlling arousal [4].…”

Section: Introductionmentioning

confidence: 99%

Modeling the role of the thalamus in resting-state functional connectivity: nature or structure

Cabrera-Álvarez¹,

Doorn²,

Maestú³

et al. 2023

Preprint

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The thalamus is a central brain structure that serves as a relay station for sensory inputs from the periphery to the cortex and regulates cortical arousal. Traditionally, it has been regarded as a passive relay that transmits information between brain regions. However, recent studies have suggested that the thalamus may also play a role in shaping functional connectivity (FC) in a task-based context. Based on this idea, we hypothesized that due to its centrality in the network and its involvement in cortical activation, the thalamus may also contribute to resting-state FC, a key neurological biomarker widely used to characterize brain function in health and disease. To investigate this hypothesis, we constructed ten in-silico brain network models based on neuroimaging data (MEG, MRI, and dwMRI), and simulated them including and excluding the thalamus. and raising the noise into thalamus to represent the afferences related to the reticular activating system (RAS) and the relay of peripheral sensory inputs. We simulated brain activity and compared the resulting FC to their empirical MEG counterparts to evaluate model's performance. Results showed that a parceled version of the thalamus with higher noise, able to drive damped cortical oscillators, enhanced the match to empirical FC. However, with an already active self-oscillatory cortex, no impact on the dynamics was observed when introducing the thalamus. We also demonstrated that the enhanced performance was not related to the structural connectivity of the thalamus, but to its higher noisy inputs. Additionally, we highlighted the relevance of a balanced signal-to-noise ratio in thalamus to allow it to propagate its own dynamics. In conclusion, our study sheds light on the role of the thalamus in shaping brain dynamics and FC in resting-state and allowed us to discuss the general role of criticality in the brain at the mesoscale level.

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The human thalamus orchestrates neocortical oscillations during NREM sleep

Cited by 40 publications

References 77 publications

Human thalamic recordings reveal that epileptic spikes block sleep spindle production during non-rapid eye movement sleep

Human thalamic recordings reveal that epileptic spikes block sleep spindle production during non-rapid eye movement sleep

Respiration shapes sleep-oscillations and memory reactivation in humans

Modeling the role of the thalamus in resting-state functional connectivity: nature or structure

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