Hippocampal Network Oscillations Rescue Memory Consolidation Deficits Caused by Sleep Loss

Ognjanovski, Nicolette; Broussard, Christopher; Żochowski, Michał; Aton, Sara J.

doi:10.1093/cercor/bhy174

Cited by 70 publications

(164 citation statements)

References 77 publications

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“…Our findings are further supported by studies that found that targeting and activation of parvalbumin interneurons at specific stimulation frequencies could ameliorate spatial learning deficits. For example, rhythmic PV interneuron activation in the hippocampal CA1 in sleep‐deprived animals during non‐REM sleep improved performance in memory tasks . Because seizures in IHKA mice can occur during all brain states, with a majority (~90%) arising from a non‐theta state, animals in our present study likely received some light activation of PV interneurons during non‐REM sleep at a theta frequency (~7 Hz) similar to that used in the described study .…”

Section: Discussionmentioning

confidence: 74%

“…For example, rhythmic PV interneuron activation in the hippocampal CA1 in sleep-deprived animals during non-REM sleep improved performance in memory tasks. 33 Because seizures in IHKA mice can occur during all brain states, with a majority (~90%) arising from a non-theta state, 34 animals in our present study likely received some light activation of PV interneurons during non-REM sleep at a theta frequency (~7 Hz) similar to that used in the described study. 33 Rhythmic activation of PV interneurons has been shown to have therapeutic effects in the gamma frequency as well.…”

Section: Pv Interneuron Stimulation and Improved Cognitionmentioning

confidence: 83%

“…33 Because seizures in IHKA mice can occur during all brain states, with a majority (~90%) arising from a non-theta state, 34 animals in our present study likely received some light activation of PV interneurons during non-REM sleep at a theta frequency (~7 Hz) similar to that used in the described study. 33 Rhythmic activation of PV interneurons has been shown to have therapeutic effects in the gamma frequency as well. This stimulation paradigm has been shown to reduce the pathology in a model of Alzheimer disease, by activating glial responses.…”

Section: Pv Interneuron Stimulation and Improved Cognitionmentioning

confidence: 83%

“…16 Fourth, it is unknown if targeting seizures is required for the beneficial effects in learning and memory or if random or periodic PV activation could also work, especially considering experimental results indicating that PV interneuron activation itself can improve different pathologies. 33,36 Fifth, the long-term effects of closed-loop intervention and optogenetic stimulation will need to be determined, that is, whether the beneficial effects of the closedloop seizure suppression end immediately after the end of the treatment, or if there are any lasting effects on seizures or cognitive ability. Sixth, it should be noted that it is not yet entirely clear whether unilateral optogenetic intervention in this paradigm achieves curtailment of seizures primarily by exciting the somata, dendrites, or axon terminals of those ipsilateral PV cells that survived the kainate administration ( Figure S1), despite being greatly reduced in number, 37,38 and/or by activating the ipsilateral axon terminals of contralaterally located PV cells that have been shown recently to undergo a prominent sprouting response after IHKA treatment.…”

Section: Limitations Of the Current Results And Their Implications mentioning

confidence: 99%

“…For example, seizure suppression was achieved not only by PV interneuron activation, but also by inhibition of principal neurons in the dorsal hippocampus . Fourth, it is unknown if targeting seizures is required for the beneficial effects in learning and memory or if random or periodic PV activation could also work, especially considering experimental results indicating that PV interneuron activation itself can improve different pathologies . Fifth, the long‐term effects of closed‐loop intervention and optogenetic stimulation will need to be determined, that is, whether the beneficial effects of the closed‐loop seizure suppression end immediately after the end of the treatment, or if there are any lasting effects on seizures or cognitive ability.…”

Section: Discussionmentioning

confidence: 99%

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Optogenetic intervention of seizures improves spatial memory in a mouse model of chronic temporal lobe epilepsy

et al. 2020

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Objective To determine if closed‐loop optogenetic seizure intervention, previously shown to reduce seizure duration in a well‐established mouse model chronic temporal lobe epilepsy (TLE), also improves the associated comorbidity of impaired spatial memory. Methods Mice with chronic, spontaneous seizures in the unilateral intrahippocampal kainic acid model of TLE, expressing channelrhodopsin in parvalbumin‐expressing interneurons, were implanted with optical fibers and electrodes, and tested for response to closed‐loop light intervention of seizures. Animals that responded to closed‐loop optogenetic curtailment of seizures were tested in the object location memory test and then given closed‐loop optogenetic intervention on all detected seizures for 2 weeks. Following this, they were tested with a second object location memory test, with different objects and contexts than used previously, to assess if seizure suppression can improve deficits in spatial memory. Results Animals that received closed‐loop optogenetic intervention performed significantly better in the second object location memory test compared to the first test. Epileptic controls with no intervention showed stable frequency and duration of seizures, as well as stable spatial memory deficits, for several months after the precipitating insult. Significance Many currently available treatments for epilepsy target seizures but not the associated comorbidities, therefore there is a need to investigate new potential therapies that may be able to improve both seizure burden and associated comorbidities of epilepsy. In this study, we showed that optogenetic intervention may be able to both shorten seizure duration and improve cognitive outcomes of spatial memory.

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Section: Discussionmentioning

confidence: 74%

Section: Pv Interneuron Stimulation and Improved Cognitionmentioning

confidence: 83%

Section: Pv Interneuron Stimulation and Improved Cognitionmentioning

confidence: 83%

Section: Limitations Of the Current Results And Their Implications mentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Optogenetic intervention of seizures improves spatial memory in a mouse model of chronic temporal lobe epilepsy

et al. 2020

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CA3 place cells that represent a novel waking experience are preferentially reactivated during sharp wave‐ripples in subsequent sleep

Hwaun

Colgin

2019

Hippocampus

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A popular model of memory consolidation posits that recent memories stored in the hippocampus are reactivated during sleep and thereby transferred to neocortex for long‐term storage. This process is thought to occur during sharp wave‐ripples (SWRs) in nonrapid eye movement sleep (NREM). However, whether the hippocampus consolidates all recent memories in the same manner remains unclear. An efficient memory system may extract novel information from recent experiences for preferential consolidation. In the hippocampus, memories are thought to be stored initially in CA3. Therefore, CA3 place cells that encode novel experiences may be preferentially reactivated during SWRs in subsequent sleep. To test this hypothesis, we recorded CA3 place cells in rats during exposure to a familiar and a novel environment and during subsequent overnight sleep. We found that CA3 place cells that preferentially coded a novel environment showed larger firing rate increases during SWRs in NREM than place cells that preferentially coded a familiar environment. Moreover, CA3 place cell ensembles replayed trajectories from a novel environment during NREM with higher fidelity than trajectories from a familiar environment. Together, these results suggest that CA3 representations of novel experiences are preferentially processed during subsequent sleep.

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Optogenetics in chronic neurodegenerative diseases, controlling the brain with light: A systematic review

El Hajj,

Al Sagheer,

Ballout

2024

J of Neuroscience Research

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Neurodegenerative diseases are progressive disorders characterized by synaptic loss and neuronal death. Optogenetics combines optical and genetic methods to control the activity of specific cell types. The efficacy of this approach in neurodegenerative diseases has been investigated in many reviews, however, none of them tackled it systematically. Our study aimed to review systematically the findings of optogenetics and its potential applications in animal models of chronic neurodegenerative diseases and compare it with deep brain stimulation and designer receptors exclusively activated by designer drugs techniques. The search strategy was performed based on the PRISMA guidelines and the risk of bias was assessed following the Systematic Review Centre for Laboratory Animal Experimentation tool. A total of 247 articles were found, of which 53 were suitable for the qualitative analysis. Our data revealed that optogenetic manipulation of distinct neurons in the brain is efficient in rescuing memory impairment, alleviating neuroinflammation, and reducing plaque pathology in Alzheimer's disease. Similarly, this technique shows an advanced understanding of the contribution of various neurons involved in the basal ganglia pathways with Parkinson's disease motor symptoms and pathology. However, the optogenetic application using animal models of Huntington's disease, multiple sclerosis, and amyotrophic lateral sclerosis was limited. Optogenetics is a promising technique that enhanced our knowledge in the research of neurodegenerative diseases and addressed potential therapeutic solutions for managing these diseases' symptoms and delaying their progression. Nevertheless, advanced investigations should be considered to improve optogenetic tools' efficacy and safety to pave the way for their translatability to the clinic.

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Hippocampal Network Oscillations Rescue Memory Consolidation Deficits Caused by Sleep Loss

Cited by 70 publications

References 77 publications

Optogenetic intervention of seizures improves spatial memory in a mouse model of chronic temporal lobe epilepsy

Optogenetic intervention of seizures improves spatial memory in a mouse model of chronic temporal lobe epilepsy

CA3 place cells that represent a novel waking experience are preferentially reactivated during sharp wave‐ripples in subsequent sleep

Optogenetics in chronic neurodegenerative diseases, controlling the brain with light: A systematic review

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