Sleep restriction suppresses neurogenesis induced by hippocampal learning

Stanford University, Palo Alto, California, United States
Journal of Neurophysiology (Impact Factor: 2.89). 01/2006; 94(6):4224-33. DOI: 10.1152/jn.00218.2005
Source: PubMed


Sleep deprivation impairs hippocampal-dependent learning, which, in turn, is associated with increased survival of newborn cells in the hippocampus. We tested whether the deleterious effects of sleep restriction on hippocampus-dependent memory were associated with reduced cell survival in the hippocampus. We show that sleep restriction impaired hippocampus-dependent learning and abolished learning-induced neurogenesis. Animals were trained in a water maze on either a spatial learning (hippocampus-dependent) task or a nonspatial (hippocampus-independent) task for 4 days. Sleep-restricted animals were kept awake for one-half of their rest phase on each of the training days. Consistent with previous reports, animals trained on the hippocampus-dependent task expressed increased survival of newborn cells in comparison with animals trained on the hippocampus-independent task. This increase was abolished by sleep restriction that caused overall reduced cell survival in all animals. Sleep restriction also selectively impaired spatial learning while performance in the nonspatial task was, surprisingly, improved. Further analysis showed that in both training groups fully rested animals applied a spatial strategy irrespective of task requirements; this strategy interfered with performance in the nonspatial task. Conversely, in sleep-restricted animals, this preferred spatial strategy was eliminated, favoring the use of nonspatial information, and hence improving performance in the nonspatial task. These findings suggest that sleep loss altered behavioral strategies to those that do not depend on the hippocampus, concomitantly reversing the neurogenic effects of hippocampus-dependent learning.

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    • "Par ailleurs, les conditions qui augmentent la neurogenèse adulte, telles que l'expositionàexposition`expositionà des environnements enrichis ou l'exercice physique volontaire , s'accompagnentégalementaccompagnentégalement d'une amélioration des performances mnésiques dans des tâches spatiales chez les rongeurs (Nilsson et al., 1999 ;Van Praag et al., 1999 ;Van der Borght et al., 2007 ;Monteiro et al., 2014). Inversement, les conditions réduisant la neurogenèse adulte dans l'hippocampe, tels que le stress, l'ˆ age, certaines conditions pathologiques, la restriction de sommeil ou l'isolement social, entraˆınenttraˆınent des déficits de mémoire dans des tâches spatiales (Drapeau et al., 2003 ;Lu et al., 2003 ;Hairston et al., 2005 ;Montaron et al., 2006 ;Gil-Mohapel et al., 2013). Certains auteurs montrent d'ailleurs des corrélations directes entre le niveau de neurogenèse adulte hippocampique et les performances mnésiques dans différentes tâches de mémoire dépendantes de l'hippocampe (Kempermann & Gage, 2002b ;Leuner et al., 2004 ;Sisti et al., 2007 ;Epp et al., 2011a). "
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    ABSTRACT: A defining characteristic of the brain is its remarkable capacity to undergo activity-dependent functional and structural remodelling via mechanisms of plasticity that form the basis of our capacity to encode and retain memories. The prevailing model of how our brain stores new information about relationships between events or new abstract constructs suggests it resides in activity-driven modifications of synaptic strength and remodelling of neural networks brought about by cellular and molecular changes within the neurons activated during learning. To date, the idea that a form of activity-dependent synaptic plasticity known as long-term potentiation, or LTP, and the associated synaptic growth play a central role in the laying down of memories has received considerable support. Beyond this mechanism of plasticity at the synapse, adult neurogenesis, i.e. the birth and growth of new neurons, is another form of neural plasticity that occurs continuously in defined brain regions such as the dentate gyrus of the hippocampus. Here, based on work in the hippocampus, we review the processes and mechanisms of the generation and selection of new neurons in the adult brain and the accumulating evidence that supports the idea that this form of neural plasticity is essential to store and lead to retrievable hippocampal-dependent memories.
    Full-text · Article · Jan 2016 · Biologie Aujourd'hui
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    • "The observation that REM sleep is critical for the spatial learning in the Morris water maze has been confirmed by some laboratories (Youngblood et al. 1997; Guan et al. 2004; Yang et al. 2008; Li et al. 2009), but not by some others (Wang et al. 2009; Walsh et al. 2011). The apparent inconsistent findings on the consequences of sleep deprivation in the water maze may be explained by the fact that animals while undergoing training can adopt alternative behavioral learning strategies that are not necessarily dependent on the hippocampus (Bjorness et al. 2005; Hairston et al. 2005). Instead of locating the platform on the basis of the spatial cues in the testing room, animals may confer to using other strategies that do not rely on those cues. "
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    ABSTRACT: Although the exact functions of sleep remain a topic of debate, several hypotheses propose that sleep benefits neuronal plasticity, which ultimately supports brain function and cognition. For over a century, researchers have applied a wide variety of behavioral, electrophysiological, biochemical and molecular approaches to study how memory processes are promoted by sleep and perturbed by sleep loss. Interestingly, experimental studies indicate that cognitive impairments as a consequence of sleep deprivation appear to be most severe with learning and memory processes that require the hippocampus, which suggests that this brain region is particularly sensitive to the consequences of sleep loss. Moreover, recent studies in laboratory rodents indicate that sleep deprivation impairs hippocampal neuronal plasticity and memory processes by attenuating intracellular cyclic adenosine monophosphate (cAMP) - protein kinase A (PKA) signaling. Attenuated cAMP-PKA signaling can lead to a reduced activity of the transcription factor cAMP response element binding protein (CREB) and ultimately affect the expression of genes and proteins involved in neuronal plasticity and memory formation. Pharmacogenetic experiments in mice show that memory deficits following sleep deprivation can be prevented by specifically boosting cAMP signaling in excitatory neurons of the hippocampus. Given the high incidence of sleep disturbance and sleep restriction in our 24/7 society, understanding the consequences of sleep loss and unraveling the underlying molecular mechanisms is of great importance.
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    • "But mainly the notion that sleep is associated with offline network remodeling, leading to memory retention, has led researchers to link EEG changes in sleep with behavioral plasticity. Indeed, some forms of learning have been found to influence SWA (e.g., Huber et al., 2008; Mascetti et al., 2013), spindle activity (Gais, Molle, Helms, & Born, 2002), and the amount of REM sleep (e.g., Hairston et al., 2005; Smith & Rose, 1997). It is today commonly assumed that experience-dependent neural plasticity during sleep is integral to global processes of memory consolidation. "
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