Post‐training reversible inactivation of hippocampus reveals interference between memory systems

Schroeder, Jeanne L.; Wingard, Jeffrey C.; Packard, Mark G.

doi:10.1002/hipo.10024

Cited by 143 publications

(131 citation statements)

References 24 publications

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“…The significance of this dissociation in coupling patterns remains to be specifically investigated. In the rat hippocampus, posttraining pharmacological inactivation actually strengthens later caudate nucleus-dependent place finding (51), further showing that interactions between striatal and hippocampal memory systems develop during offline consolidation periods. Our results extend these animal findings by demonstrating that memory systems may interact well beyond the learning episode in humans, a process in which sleep is assigned an important role.…”

Section: Discussionmentioning

confidence: 82%

Sleep after spatial learning promotes covert reorganization of brain activity

Orban

Rauchs

Balteau

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

154

130

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Sleep promotes the integration of recently acquired spatial memories into cerebral networks for the long term. In this study, we examined how sleep deprivation hinders this consolidation process. Using functional MRI, we mapped regional cerebral activity during place-finding navigation in a virtual town, immediately after learning and 3 days later, in subjects either allowed regular sleep (RS) or totally sleep-deprived (TSD) on the first posttraining night. At immediate and delayed retrieval, place-finding navigation elicited increased brain activity in an extended hippocamponeocortical network in both RS and TSD subjects. Behavioral performance was equivalent between groups. However, striatal navigation-related activity increased more at delayed retrieval in RS than in TSD subjects. Furthermore, correlations between striatal response and behavioral performance, as well as functional connectivity between the striatum and the hippocampus, were modulated by posttraining sleep. These data suggest that brain activity is restructured during sleep in such a way that navigation in the virtual environment, initially related to a hippocampus-dependent spatial strategy, becomes progressively contingent in part on a response-based strategy mediated by the striatum. Both neural strategies eventually relate to equivalent performance levels, indicating that covert reorganization of brain patterns underlying navigation after sleep is not necessarily accompanied by overt changes in behavior.functional MRI ͉ hippocampus ͉ sleep deprivation ͉ memory consolidation ͉ striatum T he hypothesis that sleep represents a crucial, albeit not always indispensable, neurophysiological state that actively promotes learning-dependent brain plasticity (1-5) has become a main topic of interest in neuroscience. In this view, an active processing of freshly acquired memories may occur in the sleeping brain, supporting the gradual consolidation process by which labile recent memories are restructured and incorporated into stable memories for the long term (6, 7).Memories that can be consciously and symbolically expressed belong to the declarative memory system. At the neuroanatomical level, their encoding and initial maintenance rely upon the integrity of the medial temporal lobe, with the hippocampus at its core (8, 9). Episodic memory for personally experienced events set in a spatiotemporal context is defined as a subclass of declarative memory (10). Animal (11) and human (12) studies suggest that the hippocampus is involved in spatial learning, because encoding is based on a flexible knowledge of relationships between environmental cues. Hippocampus-dependent spatial memory in animals is thus phylogenetically viewed as a homologue of human episodic͞ declarative memory (13,14). However, spatial navigation in a well learned environment may also be mediated by the striatum through the expression of stimulus-response associations (15, 16). Current research further suggests that rodents (17, 18) and humans (19) tend to initially use a hippocampus-de...

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Section: Discussionmentioning

confidence: 82%

Sleep after spatial learning promotes covert reorganization of brain activity

Orban

Rauchs

Balteau

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

154

130

View full text Add to dashboard Cite

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“…Decreased hippocampal activity is known to facilitate striatal-based skills when the two systems compete to drive behavior (Middei et al, 2004;Schroeder et al, 2002). Therefore, impaired hippocampal function in Oprd1 À / À mice may account for their ameliorated performance in response and skill learning tasks, via altered HPC-striatum balance in favor of the striatum (Ciamei and Morton, 2009).…”

Section: Discussionmentioning

confidence: 99%

Impaired Hippocampus-Dependent and Facilitated Striatum-Dependent Behaviors in Mice Lacking the Delta Opioid Receptor

Merrer

Rezaï

Scherrer

et al. 2013

Neuropsychopharmacol

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Pharmacological data suggest that delta opioid receptors modulate learning and memory processes. In the present study, we investigated whether inactivation of the delta opioid receptor modifies hippocampus (HPC)-and striatum-dependent behaviors. We first assessed HPC-dependent learning in mice lacking the receptor (Oprd1 À / À mice) or wild-type (WT) mice treated with the delta opioid antagonist naltrindole using novel object recognition, and a dual-solution cross-maze task. Second, we subjected mutant animals to memory tests addressing striatum-dependent learning using a single-solution response cross-maze task and a motor skill-learning task. Genetic and pharmacological inactivation of delta opioid receptors reduced performance in HPC-dependent object place recognition. Place learning was also altered in Oprd1 À / À animals, whereas striatum-dependent response and procedural learning were facilitated. Third, we investigated the expression levels for a large set of genes involved in neurotransmission in both HPC and striatum of Oprd1 À / À mice. Gene expression was modified for several key genes that may contribute to alter hippocampal and striatal functions, and bias striatal output towards striatonigral activity. To test this hypothesis, we finally examined locomotor effects of dopamine receptor agonists. We found that Oprd1 À / À and naltrindole-treated WT mice were more sensitive to the stimulant locomotor effect of SKF-81297 (D1/D5), supporting the hypothesis of facilitated striatonigral output. These data suggest, for the first time, that delta receptor activity tonically inhibits striatal function, and demonstrate that delta opioid receptors modulate learning and memory performance by regulating the HPC/striatum balance.

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“…Therefore, the enhancement of one aspect of the memory may prevent the enhancement of another aspect. Competitive interactions between memories are thought to occur during encoding (Poldrack and Packard 2003); they may also occur during consolidation (Schroeder et al 2002). …”

Section: Discussionmentioning

confidence: 99%

Motor sequence consolidation: constrained by critical time windows or competing components

Cohen

Robertson

2006

Exp Brain Res

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Skill improvements may develop between practice sessions during memory consolidation. Skill enhancement within an egocentric coordinate frame develops over wake, whereas skill enhancement in an allocentric coordinate frame develops over a night of sleep. We tested whether both types of improvement could develop over two different 24-hr intervals: 8am to 8am or from 8pm to 8pm. We found that for each 24 hour interval, only one type of skill improvement was seen. Despite passing through wake and a night of sleep participants only showed skill improvements commensurate with either a night of sleep or a day awake. The nature of the off-line skill enhancement was determined by when consolidation occurred within the normal sleep-wake cycle. We conclude that motor sequence consolidation is constrained either by having critical time windows or by a competitive interaction in which improvements within one coordinate frame actively block improvements from developing in the alternative coordinate frame.

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Post‐training reversible inactivation of hippocampus reveals interference between memory systems

Cited by 143 publications

References 24 publications

Sleep after spatial learning promotes covert reorganization of brain activity

Sleep after spatial learning promotes covert reorganization of brain activity

Impaired Hippocampus-Dependent and Facilitated Striatum-Dependent Behaviors in Mice Lacking the Delta Opioid Receptor

Motor sequence consolidation: constrained by critical time windows or competing components

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