Detection of a Temporal Error Triggers Reconsolidation of Amygdala-Dependent Memories

Díaz-Mataix, Lorenzo; Martinez, Raquel Chacon Ruiz; Schafe, Glenn E.; LeDoux, Joseph E.; Doyère, Valérie

doi:10.1016/j.cub.2013.01.053

Cited by 144 publications

(168 citation statements)

References 25 publications

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“…Hence, these results strengthened the hypothesis that US temporal error detection is critical to trigger memory destabilization, rather than the mere reactivation of the already consolidated memory; and they are also consistent with a recent report by Díaz-Mataix et al (2013). However, in that report, temporal control of behavior was not precise and thus it is unclear whether the amnestic altered memory strength or temporal control.…”

Section: Methodssupporting

confidence: 80%

“…This suggests the existence of different expectations about US arrival as a function of training parameters (also see Savastano and Miller 1998). Then, by varying the temporal expectation of the US presentation during reinforced reactivations (CS -US) and using MDZ as an amnestic agent, we replicated the aforementioned results of Díaz-Mataix et al (2013), showing that US temporal prediction error is critical for memory destabilization-reconsolidation (Exps 2 and 3). In subsequent experiments (Exps 4 -8), by a systematic combination of both temporal-specific memories with different CS-reactivation lengths, we demonstrated that the necessary time to reveal these four possible outcomes (mere retrieval, destabilization-reconsolidation, transitional insensitive period, and extinction) from a post-training CS presentation is highly dependent on the conditions established during training.…”

supporting

confidence: 71%

“…We first observed that the induction of an US temporal prediction error can occur when the US was presented during memory reactivation, provided that the temporal parameters of training were altered during retraining (Díaz-Mataix et al 2013). This demonstrated that a difference between what is expected and what is experienced (i.e., US temporal prediction error) is critical for memory destabilization and subsequent reconsolidation.…”

Section: Discussionmentioning

confidence: 99%

“…First, as previously suggested, time is encoded as a component of associative memories and critically determines the timing of conditioned responding, possibly through temporal predictions about the reinforcer onset (Savastano and Miller 1998;Gallistel and Balsam 2014). In addition, US temporal prediction-error determines the extent to which reactivation destabilizes a memory trace thus making it vulnerable to the effects of an amnestic agent (Díaz-Mataix et al 2013). Second, whichever of four possible outcomes occurs after memory reactivation depends on specific training conditions.…”

Section: Discussionmentioning

confidence: 99%

“…Such analyses are available in the Supplemental Material under the heading Supplementary analysis (SA). A previous study used a design in which animals were retrained under similar or different temporal parameters and subsequently administered anisomycin in the lateral amygdala (Díaz-Mataix et al 2013). Although they observed that the amnestic only exerted an effect when US timing was changed (by presenting shock before or after it was previously trained), they did not observe a precise temporal control.…”

Section: Methodsmentioning

confidence: 99%

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Prediction error and trace dominance determine the fate of fear memories after post-training manipulations

et al. 2015

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Different mnemonic outcomes have been observed when associative memories are reactivated by CS exposure and followed by amnestics. These outcomes include mere retrieval, destabilization-reconsolidation, a transitional period (which is insensitive to amnestics), and extinction learning. However, little is known about the interaction between initial learning conditions and these outcomes during a reinforced or nonreinforced reactivation. Here we systematically combined temporally specific memories with different reactivation parameters to observe whether these four outcomes are determined by the conditions established during training. First, we validated two training regimens with different temporal expectations about US arrival. Then, using Midazolam (MDZ) as an amnestic agent, fear memories in both learning conditions were submitted to retraining either under identical or different parameters to the original training. Destabilization (i.e., susceptibly to MDZ) occurred when reactivation was reinforced, provided the occurrence of a temporal prediction error about US arrival. In subsequent experiments, both treatments were systematically reactivated by nonreinforced context exposure of different lengths, which allowed to explore the interaction between training and reactivation lengths. These results suggest that temporal prediction error and trace dominance determine the extent to which reactivation produces the different outcomes.

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Section: Methodssupporting

confidence: 80%

supporting

confidence: 71%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 3 more Smart Citations

Prediction error and trace dominance determine the fate of fear memories after post-training manipulations

et al. 2015

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A crabs' high‐order brain center resolved as a mushroom body‐like structure

Maza

Sztarker

Cozzarin

et al. 2020

J of Comparative Neurology

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The hypothesis of a common origin for high-order memory centers in bilateral animals presents the question of how different brain structures, such as the vertebrate hippocampus and the arthropod mushroom bodies, are both structurally and functionally comparable. Obtaining evidence to support the hypothesis that crustaceans possess structures equivalent to the mushroom bodies that play a role in associative memories has proved challenging. Structural evidence supports that the hemiellipsoid bodies of hermit crabs, crayfish and lobsters, spiny lobsters, and shrimps are homologous to insect mushroom bodies. Although a preliminary description and functional evidence supporting such homology in true crabs (Brachyura) has recently been shown, other authors consider the identification of a possible mushroom body homolog in Brachyura as problematic. Here we present morphological and immunohistochemical data in Neohelice granulata supporting that crabs possess well-developed hemiellipsoid bodies that are resolved as mushroom bodies-like structures. Neohelice exhibits a peduncle-like tract, from which processes project into proximal and distal domains with different neuronal specializations. The proximal domains exhibit spines and en passant-like processes and are proposed here as regions mainly receiving inputs. The distal domains exhibit a "trauben"-like compartmentalized structure with bulky terminal specializations and are proposed here as output regions. In addition, we found microglomeruli-like complexes, adult neurogenesis, aminergic innervation, and elevated expression of proteins necessary for memory processes. Finally, in vivo calcium imaging suggests that, as in insect mushroom bodies, the output regions exhibit stimulus-specific activity. Our results support the shared organization of memory centers across crustaceans and insects.

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Investigating Memory Updating in Mice Using the Objects in Updated Locations Task

2020

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In the laboratory, memory is typically studied as a de novo experience, in which a naïve animal is exposed to a discrete learning event that is markedly different from its past experiences. Most real‐world memories, however, are updates—modifications or additions—to existing memories. This is particularly true in the aging, experienced brain. To better understand memory updating, we have developed a new behavioral paradigm called the objects in updated locations (OUL) task. OUL relies on hippocampus‐dependent spatial learning and has the advantage of being able to test both the original memory and the updated information in a single test session. Further, OUL relies on incidental learning that avoids unnecessary stress that might hinder the performance of aging animals. In OUL, animals first learn the location of two identical objects in a familiar context. This memory is then updated by moving one object to a new location. Finally, to assess the animals’ memory for the original and the updated information, all animals are given a test session in which they are exposed to four copies of the object: two in the original training locations, one in the updated location, and one in a novel location. By comparing exploration of the novel location to the familiar locations, we can infer whether the animal remembers the original and updated object locations. OUL is a simple but powerful task that could provide new insights into the cellular, circuit‐level, and molecular mechanisms that support memory updating. © 2020 by John Wiley & Sons, Inc.

show abstract

Detection of a Temporal Error Triggers Reconsolidation of Amygdala-Dependent Memories

Cited by 144 publications

References 25 publications

Prediction error and trace dominance determine the fate of fear memories after post-training manipulations

Prediction error and trace dominance determine the fate of fear memories after post-training manipulations

A crabs' high‐order brain center resolved as a mushroom body‐like structure

Investigating Memory Updating in Mice Using the Objects in Updated Locations Task

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