Dysrhythmia in the suprachiasmatic nucleus inhibits memory processing

Fernandez, Fabian-Xosé; Lu, D.; Ha, Phong; Costacurta, Patricia; Chavez, Renee; Heller, H. Craig; Ruby, Norman F.

doi:10.1126/science.1259652

Cited by 91 publications

(90 citation statements)

References 35 publications

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“…41,42 However, SCN lesions rescue learning deficits in arrhythmic Siberian hamsters, suggesting that an arrhythmic master circadian clock in these animals actively inhibits memory consolidation. 43 Together, these results suggest that the circadian integrity of the neuronal network within the SCN is important for normal memory consolidation. In support of this view, we have previously shown that desynchrony of sleep stages in the forced desynchronized rat emerges from the desynchrony of specific neuronal subpopulations within the SCN.…”

Section: Discussionmentioning

confidence: 81%

Fragmentation of Rapid Eye Movement and Nonrapid Eye Movement Sleep without Total Sleep Loss Impairs Hippocampus-Dependent Fear Memory Consolidation

Lee

Katsuyama

Duge

et al. 2016

Sleep

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Study Objectives: Sleep is important for consolidation of hippocampus-dependent memories. It is hypothesized that the temporal sequence of nonrapid eye movement (NREM) sleep and rapid eye movement (REM) sleep is critical for the weakening of nonadaptive memories and the subsequent transfer of memories temporarily stored in the hippocampus to more permanent memories in the neocortex. A great body of evidence supporting this hypothesis relies on behavioral, pharmacological, neural, and/or genetic manipulations that induce sleep deprivation or stage-specific sleep deprivation. Methods:We exploit an experimental model of circadian desynchrony in which intact animals are not deprived of any sleep stage but show fragmentation of REM and NREM sleep within nonfragmented sleep bouts. We test the hypothesis that the shortening of NREM and REM sleep durations post-training will impair memory consolidation irrespective of total sleep duration. Results: When circadian-desynchronized animals are trained in a hippocampus-dependent contextual fear-conditioning task they show normal short-term memory but impaired long-term memory consolidation. This impairment in memory consolidation is positively associated with the post-training fragmentation of REM and NREM sleep but is not significantly associated with the fragmentation of total sleep or the total amount of delta activity. We also show that the sleep stage fragmentation resulting from circadian desynchrony has no effect on hippocampus-dependent spatial memory and no effect on hippocampusindependent cued fear-conditioning memory. Conclusions: Our findings in an intact animal model, in which sleep deprivation is not a confounding factor, support the hypothesis that the stereotypic sequence and duration of sleep stages play a specific role in long-term hippocampus-dependent fear memory consolidation.

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Section: Discussionmentioning

confidence: 81%

Fragmentation of Rapid Eye Movement and Nonrapid Eye Movement Sleep without Total Sleep Loss Impairs Hippocampus-Dependent Fear Memory Consolidation

Lee

Katsuyama

Duge

et al. 2016

Sleep

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show abstract

“…Several animal models were applied to study the functional significance of circadian system, such as constant light exposure on rats (Fonken et al, 2012;Honma and Hiroshige, 1978), suprachiasmatic nucleus (SCN) ablation in Siberian hamsters (Bittman et al, 1991;Fernandez et al, 2014), and genetic modification of mice (Oliver et al, 2012;Vitaterna et al, 1994) and fruit flies (Konopka and Benzer, 1971;Simoni et al, 2014). Evidences indicated a strong correlation between circadian rhythms disruption and memory impairments in animal models.…”

Section: Introductionmentioning

confidence: 99%

Chronic constant light-induced hippocampal late-phase long-term potentiation impairment in vitro is attenuated by antagonist of D1/D5 receptors

Chai¹,

Ma²,

Wang³

et al. 2015

Brain Research

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“…Circadian disruption through constant light conditions (Daan and Pittendrigh 1976) decreases performance in the Morris water maze along with hippocampal neurogenesis (Fujioka et al 2011). In wild-type hamsters with the SCN intact, induction of circadian dysrhythmia impairs spatial and recognition memory (Fernandez et al 2014). Acute experimental jet lag also disrupts recall of longterm contextual fear conditioning in mice (Loh et al 2010).…”

Section: Circadian Dysfunction and Memorymentioning

confidence: 99%

“…In rats, disinhibition of recurrent GABAergic inhibition is suggested as a mechanism for regulating circadian rhythmicity of LTP in hippocampal CA1 (Nakatsuka and Natsume 2014). In hamsters, circadian rhythmicity is necessary for declarative learning and memory as increased SCN GABAergic inhibition to the hippocampus in arrhythmic animals impairs memory (Ruby et al 2008(Ruby et al , 2013Fernandez et al 2014).…”

Section: Mechanisms Linking the Circadian Clock And Memorymentioning

confidence: 99%

Synchrony and desynchrony in circadian clocks: impacts on learning and memory

Krishnan

Lyons

2015

Learn. Mem.

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Circadian clocks evolved under conditions of environmental variation, primarily alternating light dark cycles, to enable organisms to anticipate daily environmental events and coordinate metabolic, physiological, and behavioral activities. However, modern lifestyle and advances in technology have increased the percentage of individuals working in phases misaligned with natural circadian activity rhythms. Endogenous circadian oscillators modulate alertness, the acquisition of learning, memory formation, and the recall of memory with examples of circadian modulation of memory observed across phyla from invertebrates to humans. Cognitive performance and memory are significantly diminished when occurring out of phase with natural circadian rhythms. Disruptions in circadian regulation can lead to impairment in the formation of memories and manifestation of other cognitive deficits. This review explores the types of interactions through which the circadian clock modulates cognition, highlights recent progress in identifying mechanistic interactions between the circadian system and the processes involved in memory formation, and outlines methods used to remediate circadian perturbations and reinforce circadian adaptation.Circadian clocks permit organisms to anticipate recurring daily environmental events through the coordination of metabolic, physiological, and behavioral rhythms. Conservation of the core principles through which circadian oscillators are organized across eukaryotic phyla suggests strong selective pressures for both circadian clocks and the mechanisms through which circadian oscillators operate. Intracellularly, transcription/translation feedback loops involving core circadian components set the stage for transcriptional regulation of thousands of genes in individual cells and tissues (Balsalobre et al.

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Dysrhythmia in the suprachiasmatic nucleus inhibits memory processing

Cited by 91 publications

References 35 publications

Fragmentation of Rapid Eye Movement and Nonrapid Eye Movement Sleep without Total Sleep Loss Impairs Hippocampus-Dependent Fear Memory Consolidation

Fragmentation of Rapid Eye Movement and Nonrapid Eye Movement Sleep without Total Sleep Loss Impairs Hippocampus-Dependent Fear Memory Consolidation

Chronic constant light-induced hippocampal late-phase long-term potentiation impairment in vitro is attenuated by antagonist of D1/D5 receptors

Synchrony and desynchrony in circadian clocks: impacts on learning and memory

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