Focal limbic sources create the large slow oscillations of the EEG in human deep sleep

Morgan, Kyle; Hathaway, Evan; Carson, Megan; Fernandez-Corazza, Mariano; Shusterman, Roman; Luu, Phan; Tucker, Don M.

doi:10.1016/j.sleep.2021.07.028

Cited by 8 publications

(19 citation statements)

References 34 publications

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“…Additional evidence against this model comes from the functional connectivity analysis (see Figure 7), which shows that in the slow oscillation frequency range (0.5-1.5 Hz), information flows in the reverse direction; from OFC to AC (replicated in both left and right hemispheres). These findings align with previous reports that the primary generator of (endogenous) SOs is found in ventral frontal areas (Morgan et al, 2021). In the second of the proposed models (Model 2 in Figure 1), sound information would arrive at the auditory cortex via primary auditory pathways and would then be passed forward to frontal regions, which would generate slow oscillations.…”

Section: Discussionsupporting

confidence: 93%

“…Several of our analyses suggest a leftward lateralization in OFC involvement. We caution against overinterpreting these findings, as hemispheric differences in brain folding and ROI placement can affect the strength of observed signals in MEG source space; however, other studies using EEG have also found that low frequency oscillations in ventral limbic areas are more frequent on the left side (Achermann et al, 2001, Morgan et al, 2021, suggesting that a more focused analysis of lateralization may be an interesting area for future work. Finally, we opted to use standard surface-based cortical source localization models.…”

Section: Discussionmentioning

confidence: 90%

“…In the third model, as auditory information travels simultaneously through the lemniscal and non-lemniscal pathways, non-lemniscal neurons interact with arousal systems in the brainstem (possibly involving LC) and/or thalamus, which then result in diffuse changes in cortical excitability, leading to the generation of slow oscillations throughout the brain. An early auditory-like response and then stronger, later responses in the OFC then might be expected due to the previously-observed tendency for ventral limbic areas (including OFC) to generate endogenous slow oscillations (Massimini et al, 2004, Morgan et al, 2021. The fourth model is a modification of the third model, in which auditory information primarily generates the CLAS effect via the non-lemniscal auditory pathway.…”

Section: Introductionmentioning

confidence: 98%

“…The N550-P900 complex has an asymmetrical shape composed of a trough in which cortical neurons are hyperpolarized, followed by a longer rebound of cortical activity during which neurons are comparatively depolarized and thus more excitable (Latreille et al, 2020). Recent work using electrical source localization models suggests that the spontaneous K-complex, which is similar to the sensory-evoked N550-P900 complex (Halász, 2016), originates in ventral limbic cortex, including medial temporal and caudal orbitofrontal cortex (OFC) (Morgan et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

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The neurophysiology of closed-loop auditory stimulation in sleep: a magnetoencephalography study

Jourde

Merlo

Brooks

et al. 2022

Preprint

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Closed-loop auditory stimulation (CLAS) is a brain modulation technique in which sounds are timed to enhance or disrupt endogenous neurophysiological events. CLAS of slow oscillation up-states in sleep is becoming a popular tool to study and potentially enhance sleep's functions, as it can increase slow oscillations, evoke sleep spindles, and enhance memory consolidation of certain tasks. However, few studies have examined the specific neurophysiological mechanisms involved in CLAS, in part because of practical limitations to commonly-used tools. To evaluate evidence for possible models of how sound stimulation during brain up-states might generate slow oscillations, we simultaneously recorded electro- and magnetoencephalography in human participants who received auditory stimulation across sleep stages and neural oscillation phases. The results suggest that auditory information reaches ventral frontal lobe areas via non-lemniscal pathways. From there, a slow oscillation is created and propagated. We demonstrate that while the state of excitability of tissue in auditory cortex and frontal ventral regions shows some synchrony with the EEG-recorded up-states that are commonly used for CLAS, it is the state of ventral frontal regions that is most critical for slow oscillation generation. Our findings advance models of how CLAS leads to enhancement of slow oscillations, sleep spindles, and associated cognitive benefits, and offer insight into how the effectiveness of brain stimulation techniques can be improved.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionmentioning

confidence: 90%

Section: Introductionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

The neurophysiology of closed-loop auditory stimulation in sleep: a magnetoencephalography study

Jourde

Merlo

Brooks

et al. 2022

Preprint

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“…Consistent with this evolutionary anatomical analysis of collothalamic origins, and the proposal that collothalamic control is the foundation of NREM sleep, recent optogenetic studies in mice have found that the slow oscillations of NREM sleep are regulated by discharges in the claustrum ( 141 ). Furthermore, high-density EEG studies of human slow oscillations in NREM sleep in our laboratory have recently shown that these large discharges of deep NREM sleep are typically localized to ventral limbic (medial anterior temporal and hippocampal gyrus) and caudal orbital frontal regions ( 142 , 143 ). These are integral forebrain structures of the collothalamic system, with their regulatory foundations in the midbrain structures of the collicular-ventral tegmental area.…”

Section: Consolidating Implicit and Explicit Forms Of Memory In Sleepmentioning

confidence: 99%

Neurophysiological mechanisms of implicit and explicit memory in the process of consciousness

Tucker

Luu

Johnson

2022

Journal of Neurophysiology

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Neurophysiological mechanisms are increasingly understood to constitute the foundations of human conscious experience. These include the capacity for ongoing memory, achieved through a hierarchy of reentrant cross-laminar connections across limbic, heteromodal, unimodal, and primary cortices. The neurophysiological mechanisms of consciousness also include the capacity for volitional direction of attention to the ongoing cognitive process, through a reentrant fronto-thalamo-cortical network regulation of the inhibitory thalamic reticular nucleus. More elusive is the way that discrete objects of subjective experience - such as the color of deep blue or the sound of middle C - could be generated by neural mechanisms. Explaining such ineffable qualities of subjective experience is what Chalmers has called "the hard problem of consciousness," which has divided modern neuroscientists and philosophers alike. We propose that insight into the appearance of the hard problem can be gained through integrating classical phenomenological studies of experience with recent progress in the differential neurophysiology of consolidating explicit versus implicit memory. Although the achievement of consciousness - once it is reflected upon - becomes explicit, the underlying process of generating consciousness, through neurophysiological mechanisms, is largely implicit. Studying the neurophysiological mechanisms of adaptive implicit memory, including brainstem, limbic, and thalamic regulation of neocortical representations, may lead to a more extended phenomenological understanding of both the neurophysiological process and the subjective experience of consciousness.

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Continuity and change in neural plasticity through embryonic morphogenesis, fetal activity‐dependent synaptogenesis, and infant memory consolidation

Luu,

Tucker

2023

Developmental Psychobiology

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There is an apparent continuity in human neural development that can be traced to venerable themes of vertebrate morphogenesis that have shaped the evolution of the reptilian telencephalon (including both primitive three‐layered cortex and basal ganglia) and then the subsequent evolution of the mammalian six‐layered neocortex. In this theoretical analysis, we propose that an evolutionary–developmental analysis of these general morphogenetic themes can help to explain the embryonic development of the dual divisions of the limbic system that control the dorsal and ventral networks of the human neocortex. These include the archicortical (dorsal limbic) Papez circuits regulated by the hippocampus that organize spatial, contextual memory, as well as the paleocortical (ventral limbic) circuits that organize object memory. We review evidence that these dorsal and ventral limbic divisions are controlled by the differential actions of brainstem lemnothalamic and midbrain collothalamic arousal control systems, respectively, thereby traversing the vertebrate subcortical neuraxis. These dual control systems are first seen shaping the phyletic morphogenesis of the archicortical and paleocortical foundations of the forebrain in embryogenesis. They then provide dual modes of activity‐dependent synaptic organization in the active (lemnothalamic) and quiet (collothalamic) stages of fetal sleep. Finally, these regulatory systems mature to form the major systems of memory consolidation of postnatal development, including the rapid eye movement (lemnothalamic) consolidation of implicit memory and social attachment in the first year, and then—in a subsequent stage—the non‐REM (collothalamic) consolidation of explicit memory that is integral to the autonomy and individuation of the second year of life.

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Focal limbic sources create the large slow oscillations of the EEG in human deep sleep

Cited by 8 publications

References 34 publications

The neurophysiology of closed-loop auditory stimulation in sleep: a magnetoencephalography study

The neurophysiology of closed-loop auditory stimulation in sleep: a magnetoencephalography study

Neurophysiological mechanisms of implicit and explicit memory in the process of consciousness

Continuity and change in neural plasticity through embryonic morphogenesis, fetal activity‐dependent synaptogenesis, and infant memory consolidation

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