Differential learning‐stage dependent patterns of c‐Fos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice

Bertaina-Anglade, Valérie; Tramu, G.; Destrade, Claude

doi:10.1046/j.1460-9568.2000.00258.x

Cited by 79 publications

(56 citation statements)

References 62 publications

(57 reference statements)

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“…Within the context of this framework, there is evidence that parallels cellular and molecular consolidation processes necessary for gene transcription and protein synthesis after induction of LTP in this region. For example, increased expression of LTP-related immediate early genes (i.e., BDNF, zif268, c-FOS, and JUNB) in dorsal CA1 has been observed within 24 hr after the exposure to learning (Frey et al, 1991;Bertaina-Anglade et al, 2000;Gusev et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

“…There is strong evidence suggesting the CA1 subregion plays a significant role in intermediate/long-term spatial memory and consolidation, but not short-term acquisition or encoding processes (O'Reilly and McClelland, 1994;Treves and Rolls, 1994;Maren et al, 1997;Bertaina-Anglade et al, 2000;Kesner et al, 2004;Lee and Kesner, 2004a;Remondes and Schuman, 2004;Daumas et al, 2005;Hasselmo, 2005;Sharifzadeh et al, 2006). Encoding of information acquired in a Hebb-Williams maze or in contextual fear conditioning, using a within-days analysis, is impaired by targeted lesions to the CA3 and dentate gyrus (DG) subregions, but not from targeted lesions to the CA1 subregion.…”

Section: Introductionmentioning

confidence: 99%

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The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

2007

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Subregional analyses of the hippocampus have suggested a selective role for the CA1 subregion in intermediate/long-term spatial memory and consolidation, but not short-term acquisition or encoding processes. It remains unclear how the direct cortical projection to CA1 via the perforant path (pp) contributes to these CA1-dependent processes. It has been suggested that dopamine selectively modulates the pp projection to CA1 while having little to no effect on the Schaffer collateral (SC) projection to CA1. This series of behavioral and electro-physiological experiments takes advantage of this pharmacological dissociation to demonstrate that the direct pp inputs to CA1 are critical in CA1-dependent intermediate-term retention and retrieval function. Here we demonstrate that local infusion of the nonselective dopamine agonist, apomorphine (10, 15 μg), into the CA1 subregion of awake animals produces impairments in between-day retention and retrieval, sparing within-day encoding of a modified Hebb-Williams maze and contextual conditioning of fear. In contrast, apomorphine produces no deficits when infused into the CA3 subregion. To complement the behavioral analyses, electrophysiological data was collected. In anesthetized animals, local infusion of the same doses of apomorphine significantly modifies evoked responses in the distal dendrites of CA1 following angular bundle stimulation, but produces no significant effects in the more proximal dendritic layer following stimulation of the SC. These results support a modulatory role for dopamine in the EC-CA1, but not CA3-CA1 circuitry, and suggest the possibility of a more fundamental role for EC-CA1 synaptic transmission in terms of intermediate-term, but not short-term spatial memory.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

2007

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“…The results are expressed as mean7SEM. In order to control for a nonspecific effect of learning, BrdU-IR cells were also counted (batch 2) within the dorsolateral corner of the subventricular zone [22][23][24][25][26][27][28][29][30][31][32] …”

Section: Quantitative Evaluation Of Peroxidase Stainingmentioning

confidence: 99%

“…In this task, two phases of learning can be distinguished: an early phase during which performance improves rapidly, and a late phase during which asymptotic levels of performance are reached. These two phases seem to involve different brain processes [28][29][30][31] and, consequently, may differentially influence neurogenesis.…”

Section: Introductionmentioning

confidence: 99%

Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date

et al. 2003

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The hippocampal formation, to which new neurons are added on a daily basis throughout life, is important in spatial learning. Surviving de novo produced cells integrate into the functional circuitry, where they can influence both normal and pathological behaviors. In this study, we examined the effect of the water-maze (a hippocampal-dependent spatial task) on neurogenesis. Learning in this task can be divided into two phases, an early phase during which performance improves rapidly, and a late phase during which asymptotic levels of performance are reached. Here we demonstrate that the late phase of learning has a multifaceted effect on neurogenesis depending on the birth date of new neurons. The number of newly born cells increased contingently with the late phase and a large proportion of these cells survived for at least 4 weeks and differentiated into neurons. In contrast, late-phase learning decreased the number of newly born cells produced during the early phase. This decline in neurogenesis was positively correlated with performance in the water-maze. Thus, rats with the highest de novo cell number were less able to acquire and use spatial information than those with low numbers of new cells. These results show that learning has a complex effect on hippocampal neurogenesis, and reveals a novel mechanism through which neurogenesis may influence normal and pathological behaviors. Molecular Psychiatry (2003) 8, 974-982.

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“…Based on changes in c-fos activity, Vann et al (2000) suggested that RE plays a role in working memory. However, c-fos imaging yields complex and sometimes controversial results (e.g., Aggleton et al 2000;Bertaina-Anglade et al 2000;Jenkins et al 2003;Santin et al 2003), while the precise role of c-fos in memory formation and the underlying mechanisms remain unknown (Herrera and Robertson 1996;Zhang et al 2002). Therefore, we used a conventional (reference memory) watermaze task, known to be sensitive to dysfunction of both the hippocampal and prefrontal systems, with each system mediating different aspects of watermaze learning.…”

Section: Introductionmentioning

confidence: 99%

Neurotoxic lesions of the thalamic reuniens or mediodorsal nucleus in rats affect non-mnemonic aspects of watermaze learning

Weel¹,

Morris

2009

Brain Struct Funct

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Rats with bilateral neurotoxic reuniens (RE), mediodorsal (MD), hippocampal (HIPP) or sham (SH) lesions were tested in a standard watermaze task, together with unoperated rats. RE-rats and SH-controls readily learned to swim directly to a hidden platform. In contrast, MD-rats displayed a transient deficit characterized initially by thigmotaxis. Like in previous studies, HIPP-rats had long latencies throughout training and displayed more random swims than the other groups. In a memory probe test with the platform removed, SH-and RE-rats approached the correct location relatively directly but, whereas SH-controls persistently searched in the training quadrant, RE-rats switched to searching all over the pool. The MDgroup swam in loops to the platform, but then displayed persistent searching in the training quadrant. The HIPPgroup performed at chance. These distinct patterns indicate that, although their search strategies were different, REand MD-rats had acquired sufficient knowledge about the platform location and could recall information in the probe test. All groups performed well in a subsequent cue test with a visible platform, with RE-rats initially escaping faster than the SH-and HIPP-groups, and MD-rats improving from an initially poorer level of performance to control level. This indicates that there were no sensorimotor or motivational deficits associated with any of the lesions. In conclusion, while the RE and MD nuclei seem not to be critical for the learning and memory of a standard watermaze task, they may contribute to non-mnemonic strategy shifting when animals are challenged in ways that do not occur during training.

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Differential learning‐stage dependent patterns of c‐Fos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice

Cited by 79 publications

References 62 publications

The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

The role of the direct perforant path input to the CA1 subregion of the dorsal hippocampus in memory retention and retrieval

Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date

Neurotoxic lesions of the thalamic reuniens or mediodorsal nucleus in rats affect non-mnemonic aspects of watermaze learning

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