Qualitatively Different Hippocampal Subfield Engagement Emerges with Mastery of a Spatial Memory Task by Rats

Poirier, Guillaume L.; Amin, Eman; Aggleton, John Patrick

doi:10.1523/jneurosci.4607-07.2008

Cited by 64 publications

(70 citation statements)

References 90 publications

(110 reference statements)

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“…Here, the differential temporal dynamics of CREB phosphorylation observed in CA1 (biphasic) and CA3 (monophasic) areas are consistent with previous findings reporting differential hippocampal subfields engagement according to the demands and the degree of mastery of a spatial task. In particular, this is consistent with the notion that CA3 may be important for the encoding of spatial information, whereas CA1 may rather be engaged in the maintenance of spatial representations and consolidation (Brun et al 2002) or retrieval processes (Kesner et al 2004;Remondes and Schuman 2004;Poirier et al 2008).…”

Section: Behaviorsupporting

confidence: 88%

Spatial memory in the Morris water maze and activation of cyclic AMP response element-binding (CREB) protein within the mouse hippocampus

Porte¹,

Buhot²,

Mons³

2008

Learn. Mem.

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We investigated the spatio-temporal dynamics of learning-induced cAMP response element-binding protein activation/phosphorylation (pCREB) in mice trained in a spatial reference memory task in the water maze. Using immunohistochemistry, we examined pCREB immunoreactivity (pCREB-ir) in hippocampal CA1 and CA3 and related brain structures. During the course of spatial learning over Days 1-9, pCREB-ir progressively increased in hippocampal neurons whereas its level in the dorsal striatum decreased. No significant changes were observed in the prelimbic cortex and lateral amygdala. Mice killed at various time points after the last training session demonstrated two waves of pCREB-ir in CA1 and an early transient CREB phosphorylation in area CA3, lateral amygdala, and prelimbic cortex. We show that CREB phosphorylation and downstream gene Zif268 activation remained sustained in CA1 and CA3 for at least 24 h after extended training (Days 8-9) but not during early training (Day 3). The present results indicate that the strong CA1 CREB phosphorylation observed immediately after training was not related strictly to learning or to memory. In contrast, at 15 min after training, the changes in CA1 CREB phosphorylation state were specifically related to individual learning capability. We suggest that hippocampal-learning specificity of CREB is reflected best by duration, rather than magnitude, of CREB phosphorylation.Memory can be divided into at least two distinct forms according to its temporal and biochemical properties: short term memory (STM), which lasts no longer than a few hours, and long-term memory (LTM), which lasts from several hours to days or even longer (McGaugh 1966;Davis and Squire 1984;Matthies 1989; Bozon et al. 2003a,b). Studies in rodents have provided evidence that STM is a labile state that depends on activation and/or posttranslational modifications of preexisting molecules whereas consolidation of LTM depends on a crucial phase of gene expression and de novo protein synthesis to transform newly learned information into a permanent and stable state (Davis and Squire 1984;Dudai 1996;McGaugh 2000). Numerous studies have shown that consolidation of many types of LTM in rodents requires phosphorylation/activation of the transcription factor CREB (cAMP response element-binding protein) on Ser 133 by cAMP-or Ca 2+ -dependent protein kinase (Bernabeu et al. 1997;Izquierdo and Medina 1997;Impey et al. 1998;Taubenfeld et al. 1999;Cammarota et al. 2000Cammarota et al. , 2005Vianna et al. 2000;Izquierdo et al. 2001;Stanciu et al. 2001;Kida et al. 2002;Desmedt et al. 2003;Zhang et al. 2003;Countryman et al. 2005;Trifilieff et al. 2006;Brightwell et al. 2007). We and others recently showed that spatial memory formation was associated with increased CREB phosphorylation within the hippocampus (Mizuno et al. 2002;Colombo et al. 2003;Goldbart et al. 2003;Martel et al. 2006;Moncada and Viola 2006; Porte et al.2008). Indeed, a role for CREB in hippocampus-dependent learning was strongly supported by oligonucleotide antis...

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Section: Behaviorsupporting

confidence: 88%

Spatial memory in the Morris water maze and activation of cyclic AMP response element-binding (CREB) protein within the mouse hippocampus

Porte¹,

Buhot²,

Mons³

2008

Learn. Mem.

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“…Our results lend further support to the hypothesis that at the molecular level, long-term maintenance of spatial representations in the hippocampus requires transcriptional events in neurons, and provide evidence that the transcription factor zif268 plays an important role in this process. The formation of spatial memory presumably involves widespread cortico-hippocampal connectivity networks within which specific regions and inputs may subserve distinct but interactive processing functions (6,28,29). Damage to structures conveying information to CA1 in these networks can affect CA1 place cell stability (30)(31)(32)(33)(34).…”

Section: Discussionmentioning

confidence: 99%

“…Among the activity-regulated transcription factors, zif268, a member of the Egr family, is best characterized by its role in synaptic plasticity and memory consolidation. Zif268 is rapidly induced in association with long-term potentiation (LTP) and in defined brain structures and circuits after specific learning experiences (1)(2)(3)(4)(5)(6). Furthermore, mutant mice with targeted inactivation of the zif268 gene cannot maintain latephase LTP in the dentate gyrus of the hippocampus and fail to form long-lasting memories (7), with particular sensitivity in hippocampal-dependent spatial memory tasks (8).…”

mentioning

confidence: 99%

Impaired long-term stability of CA1 place cell representation in mice lacking the transcription factor zif268 / egr1

Renaudineau

Poucet

Laroche

et al. 2009

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

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Zif268 is a transcriptional regulator that plays a crucial role in maintenance of the late phases of hippocampal long-term potentiation (LTP) and consolidation of spatial memories. Because the hippocampal place cell system is essential for long-term spatial memory, we tested the hypothesis that zif268 is required for long-term stability of hippocampal place cell representations by recording CA1 place cells in mice lacking zif268. We found that zif268 gene deletion destabilized the representation of a familiar environment after exposure to a novel environment and impaired the long-term (24 h), but not short-term (1 h), stability of newly formed representations. These impairments could be rescued by repeated exposure to the novel environment, however. These results indicate that zif268 contributes to the long-term stability of spatial representations in CA1 and support the notion that the long-term stability of place cell representations requires transcriptiondependent mechanisms similar to those observed in LTP.hippocampus ͉ spatial memory

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“…The apparatus consisted of an elevated radial maze. 40 Eight arms (65 cm long × 12 cm wide) ended by rectangular platforms (17 cm × 25 cm) were arranged around an octagonal central platform (33 cm diameter). Each arm could be automatically moved in an upward (open) or a downward position (close) by the experimenter monitoring rat movements using a video camera above the maze while located in a room directly adjacent to the testing room.…”

Section: Behavioral Apparatusmentioning

confidence: 99%

Levels of Interference in Long and Short-Term Memory Differentially Modulate Non-REM and REM Sleep

Fraize

Carponcy

Joseph

et al. 2016

Sleep

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Study Objectives: It is commonly accepted that sleep is beneficial to memory processes, but it is still unclear if this benefit originates from improved memory consolidation or enhanced information processing. It has thus been proposed that sleep may also promote forgetting of undesirable and non-essential memories, a process required for optimization of cognitive resources. We tested the hypothesis that non-rapid eye movement sleep (NREMS) promotes forgetting of irrelevant information, more specifically when processing information in working memory (WM), while REM sleep (REMS) facilitates the consolidation of important information. Methods: We recorded sleep patterns of rats trained in a radial maze in three different tasks engaging either the long-term or short-term storage of information, as well as a gradual level of interference. Results: We observed a transient increase in REMS amount on the day the animal learned the rule of a long-term/reference memory task (RM), and, in contrast, a positive correlation between the performance of rats trained in a WM task involving an important processing of interference and the amount of NREMS or slow wave activity. Various oscillatory events were also differentially modulated by the type of training involved. Notably, NREMS spindles and REMS rapid theta increase with RM training, while sharp-wave ripples increase with all types of training. Conclusions: These results suggest that REMS, but also rapid oscillations occurring during NREMS would be specifically implicated in the long-term memory in RM, whereas NREMS and slow oscillations could be involved in the forgetting of irrelevant information required for WM.

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Qualitatively Different Hippocampal Subfield Engagement Emerges with Mastery of a Spatial Memory Task by Rats

Cited by 64 publications

References 90 publications

Spatial memory in the Morris water maze and activation of cyclic AMP response element-binding (CREB) protein within the mouse hippocampus

Spatial memory in the Morris water maze and activation of cyclic AMP response element-binding (CREB) protein within the mouse hippocampus

Impaired long-term stability of CA1 place cell representation in mice lacking the transcription factor zif268 / egr1

Levels of Interference in Long and Short-Term Memory Differentially Modulate Non-REM and REM Sleep

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