Moderate Cortical Cooling Eliminates Thalamocortical Silent States during Slow Oscillation

During non-rapid eye movement sleep and certain types of anaesthesia, neurons in the neocortex and thalamus exhibit a distinctive slow (<1 Hz) oscillation that consists of alternating UP and DOWN membrane potential states and which correlates with a pronounced slow (<1 Hz) rhythm in the electroencephalogram. While several studies have claimed that the slow oscillation is generated exclusively in neocortical networks and then transmitted to other brain areas, substantial evidence exists to suggest that the full expression of the slow oscillation in an intact thalamocortical (TC) network requires the balanced interaction of oscillator systems in both the neocortex and thalamus. Within such a scenario, we have previously argued that the powerful low-threshold Ca 2+ potential (LTCP)-mediated burst of action potentials that initiates the UP states in individual TC neurons may be a vital signal for instigating UP states in related cortical areas. To investigate these issues we constructed a computational model of the TC network which encompasses the important known aspects of the slow oscillation that have been garnered from earlier in vivo and in vitro experiments. Using this model we confirm that the overall expression of the slow oscillation is intricately reliant on intact connections between the thalamus and the cortex. In particular, we demonstrate that UP state-related LTCP-mediated bursts in TC neurons are proficient in triggering synchronous UP states in cortical networks, thereby bringing about a synchronous slow oscillation in the whole network. The importance of LTCP-mediated action potential bursts in the slow oscillation is also underlined by the observation that their associated dendritic Ca 2+ signals are the only ones that inform corticothalamic synapses of the TC neuron output, since they, but not those elicited by tonic action potential firing, reach the distal dendritic sites where these synapses are located.

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Ultra-slow oscillation (0.025 Hz) triggers hippocampal afterdischarges in Wistar rats

Neuroscience ◽

10.1016/s0306-4522(99)00367-x ◽

1999 ◽

Vol 94 (3) ◽

pp. 735-743 ◽

Cited By ~ 49

Author(s):

M Penttonen ◽

N Nurminen ◽

R Miettinen ◽

J Sirviö ◽

D.A Henze ◽

...

Keyword(s):

Wistar Rats ◽

Slow Oscillation

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Focal Cortical Cooling

Neurological Disease and Therapy - Epilepsy Surgery ◽

10.1201/b14113-77 ◽

2005 ◽

pp. 820-827

Author(s):

Steven Rothman ◽

Xiao-Feng Yang

Keyword(s):

Cortical Cooling

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Functional Structure of Spontaneous Sleep Slow Oscillation Activity in Humans

PLoS ONE ◽

10.1371/journal.pone.0007601 ◽

2009 ◽

Vol 4 (10) ◽

pp. e7601 ◽

Cited By ~ 39

Author(s):

Danilo Menicucci ◽

Andrea Piarulli ◽

Ursula Debarnot ◽

Paola d'Ascanio ◽

Alberto Landi ◽

...

Keyword(s):

Slow Oscillation ◽

Functional Structure

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Desynchronization of slow oscillations in the basal ganglia during natural sleep

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1720795115 ◽

2018 ◽

Vol 115 (18) ◽

pp. E4274-E4283 ◽

Cited By ~ 7

Author(s):

Aviv D. Mizrahi-Kliger ◽

Alexander Kaplan ◽

Zvi Israel ◽

Hagai Bergman

Keyword(s):

Basal Ganglia ◽

Field Potential ◽

Slow Oscillation ◽

Oscillatory Activity ◽

Neuronal Cultures ◽

Vervet Monkeys ◽

Slow Oscillations ◽

Natural Sleep ◽

Sleep Physiology ◽

Local Circuits

Slow oscillations of neuronal activity alternating between firing and silence are a hallmark of slow-wave sleep (SWS). These oscillations reflect the default activity present in all mammalian species, and are ubiquitous to anesthesia, brain slice preparations, and neuronal cultures. In all these cases, neuronal firing is highly synchronous within local circuits, suggesting that oscillation–synchronization coupling may be a governing principle of sleep physiology regardless of anatomical connectivity. To investigate whether this principle applies to overall brain organization, we recorded the activity of individual neurons from basal ganglia (BG) structures and the thalamocortical (TC) network over 70 full nights of natural sleep in two vervet monkeys. During SWS, BG neurons manifested slow oscillations (∼0.5 Hz) in firing rate that were as prominent as in the TC network. However, in sharp contrast to any neural substrate explored thus far, the slow oscillations in all BG structures were completely desynchronized between individual neurons. Furthermore, whereas in the TC network single-cell spiking was locked to slow oscillations in the local field potential (LFP), the BG LFP exhibited only weak slow oscillatory activity and failed to entrain nearby cells. We thus show that synchrony is not inherent to slow oscillations, and propose that the BG desynchronization of slow oscillations could stem from its unique anatomy and functional connectivity. Finally, we posit that BG slow-oscillation desynchronization may further the reemergence of slow-oscillation traveling waves from multiple independent origins in the frontal cortex, thus significantly contributing to normal SWS.

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044 Slow oscillatory transcranial direct current stimulation enhances cognitive performance during subsequent sleep deprivation

SLEEP ◽

10.1093/sleep/zsab072.043 ◽

2021 ◽

Vol 44 (Supplement_2) ◽

pp. A19-A19

Author(s):

John Hughes ◽

Tracy Jill Doty ◽

Ruthie Ratcliffe ◽

Thomas Balkin

Keyword(s):

Sleep Deprivation ◽

Cognitive Performance ◽

Direct Current ◽

Transcranial Direct Current Stimulation ◽

Slow Oscillation ◽

Physiological Basis ◽

Medicine Research ◽

Direct Current Stimulation ◽

Psychomotor Vigilance Test ◽

Recovery Sleep

Abstract Introduction The EEG slow oscillation of < 1 Hertz frequency has been implicated in various sleep functions, sparking a recent interest in slow oscillation enhancement strategies. In a seminal study, Marshall et al. (2006) demonstrated that 25 minutes of a slow oscillatory form of transcranial direct current stimulation (SO-tDCS) during early nocturnal sleep improved subsequent retention of word pairs learned prior to sleep, consistent with a proposed role for the slow oscillation in sleep-related memory consolidation. Another proposed function of the slow oscillation is synaptic downscaling, hypothesized to constitute the physiological basis for satisfying the homeostatic drive for sleep, per the synaptic homeostasis hypothesis of Tononi and Cirelli. We sought to determine if SO-tDCS could enhance the restorative properties of sleep, by enhancing slow oscillation activity, during a restricted sleep opportunity by assessing performance during a subsequent period of sleep deprivation (SD). Methods Twenty-six healthy volunteers were randomized into two groups. Participants either received electrical stimulation with 50 minutes of SO-tDCS at 0.75Hz, or sham stimulation, during the second hour of a restricted two hour sleep opportunity (11:00PM TO 1:00AM), followed by a 46 hour period of SD and then two recovery nights of sleep. Vigilance was assessed periodically with the Psychomotor Vigilance Test (PVT) during a baseline day, SD, and during the two days following recovery sleep nights. Results A mixed linear regression revealed significant main effects of day, group, and the interaction between group and day on mean reaction time (RT). Posthoc analysis revealed faster RTs following stimulation on day 2 of SD. It was also found that participants in the stimulation group had fewer major lapses (RTs > 500 ms) than those in the sham group over the first three days following stimulation. Conclusion Slow oscillatory transcranial direct current stimulation during a portion of a restricted period of sleep appears to enhance sleep’s restorative properties and improves cognitive performance during subsequent sustained wakefulness. The mechanistic basis for this phenomenon may be increased slow oscillation induced synaptic renormalization. Support (if any) Department of Defense Military Operational Medicine Research Program (MOMRP)

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Bidirectional Interaction of Hippocampal Ripples and Cortical Slow Waves Leads to Coordinated Spiking Activity During NREM Sleep

Cerebral Cortex ◽

10.1093/cercor/bhaa228 ◽

2020 ◽

Vol 31 (1) ◽

pp. 324-340

Author(s):

Pavel Sanda ◽

Paola Malerba ◽

Xi Jiang ◽

Giri P Krishnan ◽

Jorge Gonzalez-Martinez ◽

...

Keyword(s):

Slow Wave ◽

Memory Consolidation ◽

Slow Wave Sleep ◽

Nrem Sleep ◽

Slow Waves ◽

Slow Oscillation ◽

Cortical Input ◽

Sharp Wave ◽

Up States ◽

Intracranial Recordings

Abstract The dialogue between cortex and hippocampus is known to be crucial for sleep-dependent memory consolidation. During slow wave sleep, memory replay depends on slow oscillation (SO) and spindles in the (neo)cortex and sharp wave-ripples (SWRs) in the hippocampus. The mechanisms underlying interaction of these rhythms are poorly understood. We examined the interaction between cortical SO and hippocampal SWRs in a model of the hippocampo–cortico–thalamic network and compared the results with human intracranial recordings during sleep. We observed that ripple occurrence peaked following the onset of an Up-state of SO and that cortical input to hippocampus was crucial to maintain this relationship. A small fraction of ripples occurred during the Down-state and controlled initiation of the next Up-state. We observed that the effect of ripple depends on its precise timing, which supports the idea that ripples occurring at different phases of SO might serve different functions, particularly in the context of encoding the new and reactivation of the old memories during memory consolidation. The study revealed complex bidirectional interaction of SWRs and SO in which early hippocampal ripples influence transitions to Up-state, while cortical Up-states control occurrence of the later ripples, which in turn influence transition to Down-state.

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Precise Slow Oscillation–Spindle Coupling Promotes Memory Consolidation in Younger and Older Adults

Scientific Reports ◽

10.1038/s41598-018-36557-z ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 29

Author(s):

Beate E. Muehlroth ◽

Myriam C. Sander ◽

Yana Fandakova ◽

Thomas H. Grandy ◽

Björn Rasch ◽

...

Keyword(s):

Older Adults ◽

Memory Consolidation ◽

Slow Oscillation

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Enhancing Memory Consolidation through Slow Oscillation and Spindle Synchronization

Journal of Neuroscience ◽

10.1523/jneurosci.2512-17.2017 ◽

2017 ◽

Vol 37 (48) ◽

pp. 11517-11519 ◽

Cited By ~ 1

Author(s):

Sara Y. Kim ◽

Enmanuelle Pardilla-Delgado ◽

Sara E. Alger

Keyword(s):

Memory Consolidation ◽

Slow Oscillation

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Parallel processing of tactile information in the cerebral cortex of the cat: effect of reversible inactivation of SI on responsiveness of SII neurons

Journal of Neurophysiology ◽

10.1152/jn.1992.67.2.411 ◽

1992 ◽

Vol 67 (2) ◽

pp. 411-429 ◽

Cited By ~ 40

Author(s):

A. B. Turman ◽

D. G. Ferrington ◽

S. Ghosh ◽

J. W. Morley ◽

M. J. Rowe

Keyword(s):

Phase Locking ◽

Receptive Fields ◽

Mechanical Stimulus ◽

Glabrous Skin ◽

Mechanical Stimuli ◽

Sinusoidal Vibration ◽

Response Level ◽

Reversible Inactivation ◽

Stimulus Response ◽

Cortical Cooling

1. Localized cortical cooling was employed in anesthetized cats for the rapid reversible inactivation of the distal forelimb region within the primary somatosensory cortex (SI). The aim was to examine the responsiveness of individual neurons in the second somatosensory area (SII) in association with SI inactivation to evaluate the relative importance for tactile processing of the direct thalamocortical projection to SII and the indirect projection from the thalamus to SII via an intracortical path through SI. 2. Response features were examined quantitatively before, during, and after SI inactivation for 29 SII neurons, the tactile receptive fields of which were on the glabrous or hairy skin of the distal forelimb. Controlled mechanical stimuli that consisted of l-s trains of either sinusoidal vibration or rectangular pulses were delivered to the skin by means of small circular probes (4- to 8-mm diam). 3. Twenty-three of the 29 SII neurons (80%) showed no change in response level (in impulses per second) as a result of SI inactivation. These included seven neurons activated exclusively or predominantly by Pacinian corpuscle (PC) receptors, six that received hair follicle input, four activated by convergent input from hairy and glabrous skin, and six driven by dynamically sensitive but non-PC inputs from the glabrous skin. 4. Six SII neurons (20%), also made up of different functional classes, displayed a reduction in response to cutaneous stimuli when SI was inactivated. 5. Stimulus-response relations, constructed by plotting response level in impulses per second against the amplitude of the mechanical stimulus, showed that the effect of SI inactivation on individual neurons was consistent over the whole response range. 6. The reduced response level seen in 20% of SII neurons in association with SI inactivation cannot be attributed to direct spread of cooling from SI to the forelimb area of SII, as there was no evidence for a cooling-induced prolongation in SII spike waveforms, an effect that is known to precede any cooling-induced reduction in responsiveness. 7. As SI inactivation produced a fall in spontaneous activity in the affected SII neurons, we suggest that the inactivation removes a source of background facilitatory influence that arises in SI and affects a small proportion of SII neurons. 8. Phase-locking and therefore the precision of impulse patterning were unchanged in the responses of SII neurons to vibration during SI inactivation. This was the case whether response levels of neurons were reduced or unchanged by SI inactivation.(ABSTRACT TRUNCATED AT 400 WORDS)

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