Electrical Stimulation of the Anterior Cingulate Gyrus Induces Responses Similar to K-complexes in Awake Humans

Voysey, Zanna; Martín-López, David; Jiménez‐Jiménez, Diego; Selway, Richard; Alarcón, Gonzalo; Valentı́n, Antonio

doi:10.1016/j.brs.2015.05.006

Cited by 12 publications

(16 citation statements)

References 43 publications

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“…Our results provide a hint on how the uncertainties in our current understanding of KCs might be resolved and support our earlier results (Ioannides et al, 2017) and the results from other recent studies, claiming that KC-related activity is more prominently identified in frontal cortical areas (Colrain, 2005; Halász, 2005) along the cingulate gyrus. Critically, our results are in full agreement with the first demonstration of focal stimulation, while awake, of a specific cortical area, which seems to correspond to our dcACC1, evoking activity resembling KCs (Voysey et al, 2015). Our results, when seen in the context of numerous other studies of sleep and awake state, suggest that similar mechanisms and networks with key hubs in the ACC deal with pain, saliency detection and environmental monitoring during both sleep and awake states.…”

Section: Introductionsupporting

confidence: 91%

“…Before spindles but not before KCs a similar active inhibition is evident in rACC and pre-SMA. The opposite (active inhibition before KCs but not before spindles) is seen in dcACC1, the area showing prominent increase in higher frequencies and located where the only area in the brain from where electrical stimulation (in awake state) generates KC-like response (Voysey et al, 2015).…”

Section: Discussionmentioning

confidence: 95%

“…The results described above and in the previous sub-sections and the first conclusions drawn from them are in excellent agreement with recent literature as the examples of the previous paragraph show. Studies with intracranial electrodes are particularly supporting, including the only study where stimulation of a specific brain area (the dcACC) was causally related to KC-like activation (Voysey et al, 2015). There seemed to be just one apparent exception: in a recent paper (Mak-McCully et al, 2015), it was reported that “ Locally generated KCs were found in all sampled areas, including cingulate, ventral temporal, and occipital cortices.…”

Section: Discussionmentioning

confidence: 99%

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The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes

Ioannides¹,

Liu²,

Kostopoulos

2019

Front. Neurosci.

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The large multicomponent K-complex (KC) and the rhythmic spindle are the hallmarks of non-rapid eye movement (NREM)-2 sleep stage. We studied with magnetoencephalography (MEG) the progress of light sleep (NREM-1 and NREM-2) and emergence of KCs and spindles. Seven periods of interest (POI) were analyzed: wakefulness, the two quiet “core” periods of light sleep (periods free from any prominent phasic or oscillatory events) and four periods before and during spindles and KCs. For each POI, eight 2-s (1250 time slices) segments were used. We employed magnetic field tomography (MFT) to extract an independent tomographic estimate of brain activity from each MEG data sample. The spectral power was then computed for each voxel in the brain for each segment of each POI. The sets of eight maps from two POIs were contrasted using a voxel-by-voxel t -test. Only increased spectral power was identified in the four key contrasts between POIs before and during spindles and KCs versus the NREM2 core. Common increases were identified for all four subjects, especially within and close to the anterior cingulate cortex (ACC). These common increases were widespread for low frequencies, while for higher frequencies they were focal, confined to specific brain areas. For the pre-KC POI, only one prominent increase was identified, confined to the theta/alpha bands in a small area in the dorsal caudal part of ACC (dcACC). During KCs, the activity in this area grows in intensity and extent (in space and frequency), filling the space between the areas that expanded their low frequency activity (in the delta band) during NREM2 compared to NREM1. Our main finding is that prominent spectral power increases before NREM2 graphoelements are confined to the dcACC, and only for KCs, sharing common features with changes of activity in dcACC of the well-studied error related negativity (ERN). ERN is seen in awake state, in perceptual conflict and situations where there is a difference between expected and actual environmental or internal events. These results suggest that a KC is the sleep side of the awake state ERN, both serving their putative sentinel roles in the frame of the saliency network.

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Section: Introductionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 95%

Section: Discussionmentioning

confidence: 99%

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The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes

Ioannides¹,

Liu²,

Kostopoulos

2019

Front. Neurosci.

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“…The demonstrated activations of these medial frontal areas, in consistency with the studies on evoked KCs (Laurino et al, 2014), may therefore be proposed as the anatomical basis for cognitive functions of KCs during sleep (Ramakrishnan et al, 2012). The MCC area that is most persistent during KCs, together with the left and right MCC areas nearby, correspond to the area labeled as “dorso-caudal anterior cingulate” in a recent study with 269 epilepsy patients with implanted electrodes for recording and stimulation (Voysey et al, 2015). It was found that only in this dorso-caudal anterior cingulate area, stimulation while the patients were awake lead to responses that were highly correlated with KCs occurring during sleep for each one of the 6 patients that had electrodes implanted in this area.…”

Section: Discussionmentioning

confidence: 93%

“…The other areas are from the current study: rACC, rostral anterior cingulate cortex; MPFC, medial prefrontal cortex; DMPFC, dorsal MPFC; MCC, midcingulate cortex; sgACC, subgenual ACC; LC, locus coeruleus; DLPFC, dorsal lateral prefrontal cortex; OFC, orbitofrontal cortex; NBM, nucleus basalis of Meynert; SPL, superior parietal lobule; preCG, precentral gyrus. The dorso-caudal anterior cingulate of reference (Voysey et al, 2015) corresponds to MCC, left MCC and right MCC .…”

Section: Methodsmentioning

confidence: 99%

Using MEG to Understand the Progression of Light Sleep and the Emergence and Functional Roles of Spindles and K-Complexes

Ioannides¹,

Liu²,

Poghosyan

et al. 2017

Front. Hum. Neurosci.

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We used tomographic analysis of MEG signals to characterize regional spectral changes in the brain at sleep onset and during light sleep. We identified two key processes that may causally link to loss of consciousness during the quiet or “core” periods of NREM1. First, active inhibition in the frontal lobe leads to delta and theta spectral power increases. Second, activation suppression leads to sharp drop of spectral power in alpha and higher frequencies in posterior parietal cortex. During NREM2 core periods, the changes identified in NREM1 become more widespread, but focal increases also emerge in alpha and low sigma band power in frontal midline cortical structures, suggesting reemergence of some monitoring of internal and external environment. Just before spindles and K-complexes (KCs), the hallmarks of NREM2, we identified focal spectral power changes in pre-frontal cortex, mid cingulate, and areas involved in environmental and internal monitoring, i.e., the rostral and sub-genual anterior cingulate. During both spindles and KCs, alpha and low sigma bands increases. Spindles emerge after further active inhibition (increase in delta power) of the frontal areas responsible for environmental monitoring, while in posterior parietal cortex, power increases in low and high sigma bands. KCs are correlated with increase in alpha power in the monitoring areas. These specific regional changes suggest strong and varied vigilance changes for KCs, but vigilance suppression and sharpening of cognitive processing for spindles. This is consistent with processes designed to ensure accurate and uncorrupted memory consolidation. The changes during KCs suggest a sentinel role: evaluation of the salience of provoking events to decide whether to increase processing and possibly wake up, or to actively inhibit further processing of intruding influences. The regional spectral patterns of NREM1, NREM2, and their dynamic changes just before spindles and KCs reveal an edge effect facilitating the emergence of spindles and KCs and defining the precise loci where they might emerge. In the time domain, the spindles are seen in widespread areas of the cortex just as reported from analysis of intracranial data, consistent with the emerging consensus of a differential topography that depends on the kind of memory stored.

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Disruption of sleep macro- and microstructure in Alzheimer’s disease: overlaps between neuropsychology, neurophysiology, and neuroimaging

Kegyes-Brassai,

Pierson-Bartel,

Bolla

et al. 2024

GeroScience

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Alzheimer’s disease (AD) is the leading cause of dementia, often associated with impaired sleep quality and disorganized sleep structure. This study aimed to characterize changes in sleep macrostructure and K-complex density in AD, in relation to neuropsychological performance and brain structural changes. We enrolled 30 AD and 30 healthy control participants, conducting neuropsychological exams, brain MRI, and one-night polysomnography. AD patients had significantly reduced total sleep time (TST), sleep efficiency, and relative durations of non-rapid eye movement (NREM) stages 2 (S2), 3 (S3), and rapid eye movement (REM) sleep (p < 0.01). K-complex (KC) density during the entire sleep period and S2 (p < 0.001) was significantly decreased in AD. We found strong correlations between global cognitive performance and relative S3 (p < 0.001; r = 0.86) and REM durations (p < 0.001; r = 0.87). TST and NREM stage 1 (S1) durations showed a moderate negative correlation with amygdaloid and hippocampal volumes (p < 0.02; r = 0.51–0.55), while S3 and REM sleep had a moderate positive correlation with cingulate cortex volume (p < 0.02; r = 0.45–0.61). KC density strongly correlated with global cognitive function (p < 0.001; r = 0.66) and the thickness of the anterior cingulate cortex (p < 0.05; r = 0.45–0.47). Our results indicate significant sleep organization changes in AD, paralleling cognitive decline. Decreased slow wave sleep and KCs are strongly associated with cingulate cortex atrophy. Since sleep changes are prominent in early AD, they may serve as prognostic markers or therapeutic targets.

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Electrical Stimulation of the Anterior Cingulate Gyrus Induces Responses Similar to K-complexes in Awake Humans

Cited by 12 publications

References 43 publications

The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes

The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes

Using MEG to Understand the Progression of Light Sleep and the Emergence and Functional Roles of Spindles and K-Complexes

Disruption of sleep macro- and microstructure in Alzheimer’s disease: overlaps between neuropsychology, neurophysiology, and neuroimaging

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