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The formation and stability of recognition memory: what happens upon recall?

Davis S, Renaudineau S, Poirier R, Poucet B, Save E, Laroche S - Front Behav Neurosci (2010)

Bottom Line: Despite the force of experimental data showing this phenomenon, a number of questions have remained unanswered and no consensus has emerged as to the conditions under which a memory can be disrupted following reactivation.To date most rodent studies of reconsolidation are based on negatively reinforced memories, in particular fear-associated memories, while the storage and stability of forms of memory that do not rely on explicit reinforcement have been less often studied.We also review recent findings suggesting that some molecular mechanisms underlying consolidation of recognition memory are similarly recruited after recall to ensure memory stability, while others are more specifically engaged in consolidation or reconsolidation.

View Article: PubMed Central - PubMed

Affiliation: Centre de Neurosciences Paris-Sud, UMR 8195, Univ Paris-Sud Orsay, France.

ABSTRACT
The idea that an already consolidated memory can become destabilized after recall and requires a process of reconsolidation to maintain it for subsequent use has gained much credence over the past decade. Experimental studies in rodents have shown pharmacological, genetic, or injurious manipulation at the time of memory reactivation can disrupt the already consolidated memory. Despite the force of experimental data showing this phenomenon, a number of questions have remained unanswered and no consensus has emerged as to the conditions under which a memory can be disrupted following reactivation. To date most rodent studies of reconsolidation are based on negatively reinforced memories, in particular fear-associated memories, while the storage and stability of forms of memory that do not rely on explicit reinforcement have been less often studied. In this review, we focus on recognition memory, a paradigm widely used in humans to probe declarative memory. We briefly outline recent advances in our understanding of the processes and brain circuits involved in recognition memory and review the evidence that recognition memory can undergo reconsolidation upon reactivation. We also review recent findings suggesting that some molecular mechanisms underlying consolidation of recognition memory are similarly recruited after recall to ensure memory stability, while others are more specifically engaged in consolidation or reconsolidation. Finally, we provide novel data on the role of Rsk2, a mental retardation gene, and of the transcription factor zif268/egr1 in reconsolidation of object-location memory, and offer suggestions as to how assessing the activation of certain molecular mechanisms following recall in recognition memory may help understand the relative importance of different aspects of remodeling or updating long-lasting memories.

No MeSH data available.


Related in: MedlinePlus

Reconsolidation of spatial object-place recognition memory is impaired in zif268 mutant mice. (A) The mice were exposed to a spatial configuration of two objects for eight consecutive sessions (overtraining) on day 1 to alleviate their consolidation deficit and retention was tested 2 days later. In this condition, zif268 mutant mice had normal object-place recognition long-term memory (LTM) as they showed preferential exploration of the displaced object (n = 5; p < 0.05) as WT mice (n = 5; p < 0.05), with no significant difference between WT and mutant mice (F1,8 = 0.12; p > 0.05). (B) When zif268 mutant mice were briefly re-exposed to the familiar configuration of objects 24 h after training, post-reactivation short-term memory (PR-STM) was intact (left panel). Both WT and zif268 mutant mice preferentially explored the displaced object (p < 0.05 in each case), with no significant difference between groups (F1,8 = 1.74; p > 0.05). In contrast, post-reactivation long-term memory (PR-LTM) was impaired in zif268 mutant mice (right panel). While WT mice preferentially explored the displaced object (n = 5; p < 0.05), performance of zif268 mutant mice was not different from chance (n = 5; p > 0.05) and there was significant difference between groups (F1,8 = 6.52; p < 0.05). Ordinates: percent time spent exploring the displaced object over the time spent exploring the non-displaced object.
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Figure 2: Reconsolidation of spatial object-place recognition memory is impaired in zif268 mutant mice. (A) The mice were exposed to a spatial configuration of two objects for eight consecutive sessions (overtraining) on day 1 to alleviate their consolidation deficit and retention was tested 2 days later. In this condition, zif268 mutant mice had normal object-place recognition long-term memory (LTM) as they showed preferential exploration of the displaced object (n = 5; p < 0.05) as WT mice (n = 5; p < 0.05), with no significant difference between WT and mutant mice (F1,8 = 0.12; p > 0.05). (B) When zif268 mutant mice were briefly re-exposed to the familiar configuration of objects 24 h after training, post-reactivation short-term memory (PR-STM) was intact (left panel). Both WT and zif268 mutant mice preferentially explored the displaced object (p < 0.05 in each case), with no significant difference between groups (F1,8 = 1.74; p > 0.05). In contrast, post-reactivation long-term memory (PR-LTM) was impaired in zif268 mutant mice (right panel). While WT mice preferentially explored the displaced object (n = 5; p < 0.05), performance of zif268 mutant mice was not different from chance (n = 5; p > 0.05) and there was significant difference between groups (F1,8 = 6.52; p < 0.05). Ordinates: percent time spent exploring the displaced object over the time spent exploring the non-displaced object.

Mentions: In the second experiment to examine whether object-place recognition memory can become destabilized after recall and requires a process of reconsolidation to maintain the memory for further use, we tested zif268 mutant mice, which have been previously shown to be impaired in object memory reconsolidation (Bozon et al., 2003a). As in the Bozon and colleagues’ experiment, we first tested whether zif268 mutant mice could form a long-term object-place memory if given additional exposures to the objects in a distributed training paradigm, a precondition to examine the potential role of zif268 in reconsolidation. WT and zif268 mutant mice were given four blocks of two 5-min trials of exploration of two different objects with a within-block inter-trial interval of 5 min and a 90-min interval between blocks, and retention was measured 2 days later by moving one of the objects to a novel location. Both WT and zif268 mutant mice showed preferential exploration of the displaced object (Figure 2A), thus demonstrating the mice can form a long-term object-place memory in conditions of extended and distributed training. We were thus able to explore the effect of a brief reactivation trial (a single 5-min session with the objects in the same locations as during training), interposed at a 1-day interval between training and retention. When post-reactivation short-term memory was tested, both WT and zif268 mutant mice showed preferential exploration of the displaced object (Figure 2B, PR-STM). One day after reactivation, WT mice also explored significantly more the displaced object (Figure 2B, PR-LTM), demonstrating a similar recognition performance to that when no reactivation was interposed. In contrast, zif268 mutant mice showed equal exploration of the two objects (Figure 2B). These findings demonstrate that a consolidated and stable object-place recognition memory can again become labile after brief reactivation and zif268 mutant mice cannot in this case reconsolidate the object-place memory. Thus a zif268-dependent reconsolidation process is similarly required after an object memory or an object-place memory is recalled.


The formation and stability of recognition memory: what happens upon recall?

Davis S, Renaudineau S, Poirier R, Poucet B, Save E, Laroche S - Front Behav Neurosci (2010)

Reconsolidation of spatial object-place recognition memory is impaired in zif268 mutant mice. (A) The mice were exposed to a spatial configuration of two objects for eight consecutive sessions (overtraining) on day 1 to alleviate their consolidation deficit and retention was tested 2 days later. In this condition, zif268 mutant mice had normal object-place recognition long-term memory (LTM) as they showed preferential exploration of the displaced object (n = 5; p < 0.05) as WT mice (n = 5; p < 0.05), with no significant difference between WT and mutant mice (F1,8 = 0.12; p > 0.05). (B) When zif268 mutant mice were briefly re-exposed to the familiar configuration of objects 24 h after training, post-reactivation short-term memory (PR-STM) was intact (left panel). Both WT and zif268 mutant mice preferentially explored the displaced object (p < 0.05 in each case), with no significant difference between groups (F1,8 = 1.74; p > 0.05). In contrast, post-reactivation long-term memory (PR-LTM) was impaired in zif268 mutant mice (right panel). While WT mice preferentially explored the displaced object (n = 5; p < 0.05), performance of zif268 mutant mice was not different from chance (n = 5; p > 0.05) and there was significant difference between groups (F1,8 = 6.52; p < 0.05). Ordinates: percent time spent exploring the displaced object over the time spent exploring the non-displaced object.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 2: Reconsolidation of spatial object-place recognition memory is impaired in zif268 mutant mice. (A) The mice were exposed to a spatial configuration of two objects for eight consecutive sessions (overtraining) on day 1 to alleviate their consolidation deficit and retention was tested 2 days later. In this condition, zif268 mutant mice had normal object-place recognition long-term memory (LTM) as they showed preferential exploration of the displaced object (n = 5; p < 0.05) as WT mice (n = 5; p < 0.05), with no significant difference between WT and mutant mice (F1,8 = 0.12; p > 0.05). (B) When zif268 mutant mice were briefly re-exposed to the familiar configuration of objects 24 h after training, post-reactivation short-term memory (PR-STM) was intact (left panel). Both WT and zif268 mutant mice preferentially explored the displaced object (p < 0.05 in each case), with no significant difference between groups (F1,8 = 1.74; p > 0.05). In contrast, post-reactivation long-term memory (PR-LTM) was impaired in zif268 mutant mice (right panel). While WT mice preferentially explored the displaced object (n = 5; p < 0.05), performance of zif268 mutant mice was not different from chance (n = 5; p > 0.05) and there was significant difference between groups (F1,8 = 6.52; p < 0.05). Ordinates: percent time spent exploring the displaced object over the time spent exploring the non-displaced object.
Mentions: In the second experiment to examine whether object-place recognition memory can become destabilized after recall and requires a process of reconsolidation to maintain the memory for further use, we tested zif268 mutant mice, which have been previously shown to be impaired in object memory reconsolidation (Bozon et al., 2003a). As in the Bozon and colleagues’ experiment, we first tested whether zif268 mutant mice could form a long-term object-place memory if given additional exposures to the objects in a distributed training paradigm, a precondition to examine the potential role of zif268 in reconsolidation. WT and zif268 mutant mice were given four blocks of two 5-min trials of exploration of two different objects with a within-block inter-trial interval of 5 min and a 90-min interval between blocks, and retention was measured 2 days later by moving one of the objects to a novel location. Both WT and zif268 mutant mice showed preferential exploration of the displaced object (Figure 2A), thus demonstrating the mice can form a long-term object-place memory in conditions of extended and distributed training. We were thus able to explore the effect of a brief reactivation trial (a single 5-min session with the objects in the same locations as during training), interposed at a 1-day interval between training and retention. When post-reactivation short-term memory was tested, both WT and zif268 mutant mice showed preferential exploration of the displaced object (Figure 2B, PR-STM). One day after reactivation, WT mice also explored significantly more the displaced object (Figure 2B, PR-LTM), demonstrating a similar recognition performance to that when no reactivation was interposed. In contrast, zif268 mutant mice showed equal exploration of the two objects (Figure 2B). These findings demonstrate that a consolidated and stable object-place recognition memory can again become labile after brief reactivation and zif268 mutant mice cannot in this case reconsolidate the object-place memory. Thus a zif268-dependent reconsolidation process is similarly required after an object memory or an object-place memory is recalled.

Bottom Line: Despite the force of experimental data showing this phenomenon, a number of questions have remained unanswered and no consensus has emerged as to the conditions under which a memory can be disrupted following reactivation.To date most rodent studies of reconsolidation are based on negatively reinforced memories, in particular fear-associated memories, while the storage and stability of forms of memory that do not rely on explicit reinforcement have been less often studied.We also review recent findings suggesting that some molecular mechanisms underlying consolidation of recognition memory are similarly recruited after recall to ensure memory stability, while others are more specifically engaged in consolidation or reconsolidation.

View Article: PubMed Central - PubMed

Affiliation: Centre de Neurosciences Paris-Sud, UMR 8195, Univ Paris-Sud Orsay, France.

ABSTRACT
The idea that an already consolidated memory can become destabilized after recall and requires a process of reconsolidation to maintain it for subsequent use has gained much credence over the past decade. Experimental studies in rodents have shown pharmacological, genetic, or injurious manipulation at the time of memory reactivation can disrupt the already consolidated memory. Despite the force of experimental data showing this phenomenon, a number of questions have remained unanswered and no consensus has emerged as to the conditions under which a memory can be disrupted following reactivation. To date most rodent studies of reconsolidation are based on negatively reinforced memories, in particular fear-associated memories, while the storage and stability of forms of memory that do not rely on explicit reinforcement have been less often studied. In this review, we focus on recognition memory, a paradigm widely used in humans to probe declarative memory. We briefly outline recent advances in our understanding of the processes and brain circuits involved in recognition memory and review the evidence that recognition memory can undergo reconsolidation upon reactivation. We also review recent findings suggesting that some molecular mechanisms underlying consolidation of recognition memory are similarly recruited after recall to ensure memory stability, while others are more specifically engaged in consolidation or reconsolidation. Finally, we provide novel data on the role of Rsk2, a mental retardation gene, and of the transcription factor zif268/egr1 in reconsolidation of object-location memory, and offer suggestions as to how assessing the activation of certain molecular mechanisms following recall in recognition memory may help understand the relative importance of different aspects of remodeling or updating long-lasting memories.

No MeSH data available.


Related in: MedlinePlus