The original concept of consolidation considers that memory requires time to be fixed. Since 2000, a comparable protein-dependent re-stabilization phase, called reconsolidation, has been assumed to ...take place after memory retrieval. This consolidation/reconsolidation hypothesis, has dominated the literature for more than 50 years, despite compelling evidence that is inconsistent with it. In this review, we present an historical overview and explain how, despite serious criticisms, this hypothesis has persisted for decades and become accepted as a dogma. Based on both older and more recent evidence, we next propose the concept of memory integration which involves the linkage or embedding of new material into an already existing representation. We believe integration provides a viable explanation for retrograde amnesia in place of the consolidation/reconsolidation hypothesis. Integration can further be the basis for several major cases of memory alteration such as time dependent memory enhancement, interference, counter-conditioning, updating and other instances of memory malleability. In a final section we consider the implications this new concept may have for memory processes and its translational applications.
Proust and involuntary retrieval Gisquet-Verrier, Pascale; Riccio, David C
Frontiers in psychology,
02/2024, Letnik:
15
Journal Article
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Proust was undoubtedly a pioneer in exploring cognitive processes engaged in memory. The analysis of the episode of the madeleine, as well as the study of Proust's statements on the goals of his ...work, clearly reveal the visionary side of this author. Long before several concepts entered into mainstream scientific thought, Proust proposed, among other things, that recall was a reconstruction, that a sensory cue could provoke a memory recall, and that we should distinguish between voluntary and involuntary memory. Through numerous episodes of "
" scattered throughout his work, Proust illustrates a particular form of autobiographic memory recall: a recall that does not involve consciousness and whose starting point is an emotion provoked by a specific cue. This recall, which leads, according to Proust, to a more intense revival of the memory than voluntary recall, has only reached prominence in cognitive science more than 80 years later. Additionaly, Proust underlined the determinant role that emotion may have in this particular form of recall. On the other hand, studies on animals have shown that the presentation of a retrieval cue could induce emotional reactions followed by a facilitation of the memory retrieval associated with the cue. The existence of these data, which support Proust's proposals, should encourage the neuroscience community to further explore, in humans and animals, this form of cue elicited emotion that initiated involuntary recall of autobiographical memory.
•Post-training hippocampal lesions can be understood as a contextual change.•Contextual change effects mimic time-dependent effects of hippocampal lesions.•Temporally graded retrograde amnesia is not ...specific for episodic/contextual memory.•Consolidation concept needs to be revisited.
For more than 50 years, knowledge of memory processes has been based on the consolidation hypothesis, which postulates that new memories require time to become stabilized. Two forms of the consolidation model exist. The Cellular Consolidation concept is based upon retrograde amnesia induced by amnesic treatments, the severity of which decreases as the learning to treatment increases over minutes or hours. In contrast, The Systems Consolidation model is based on post-training hippocampal lesions, which produce more severe retrograde amnesia when induced after days than after weeks. Except for the temporal parameters, Cellular and Systems Consolidation show many similarities. Here we propose that Systems consolidation, much as Cellular Consolidation (see Gisquet- Verrier and Riccio, 2018), can be explained in terms of a form of state-dependency. Accordingly, lesions of the hippocampus induce a change in the internal state of the animal, which disrupts retrieval processes. But the effect of contextual change is known to decrease with the length of the retention intervals, consistent with time-dependent retrograde amnesia. We provide evidence supporting this new view.
•Memories for context become less specific with time, thus animals generalize fear.•Activity of the PL, IL, ACC and vHPC underlie expression of generalized fear.•Inactivation of the ACC and vHPC at ...remote testing attenuated generalized fear.•An interaction between the ACC and vHPC may control expression of generalized fear.
Memories for context become less specific with time resulting in animals generalizing fear from training contexts to novel contexts. Though much attention has been given to the neural structures that underlie the long-term consolidation of a context fear memory, very little is known about the mechanisms responsible for the increase in fear generalization that occurs as the memory ages. Here, we examine the neural pattern of activation underlying the expression of a generalized context fear memory in male C57BL/6J mice. Animals were context fear conditioned and tested for fear in either the training context or a novel context at recent and remote time points. Animals were sacrificed and fluorescent in situ hybridization was performed to assay neural activation. Our results demonstrate activity of the prelimbic, infralimbic, and anterior cingulate (ACC) cortices as well as the ventral hippocampus (vHPC) underlie expression of a generalized fear memory. To verify the involvement of the ACC and vHPC in the expression of a generalized fear memory, animals were context fear conditioned and infused with 4% lidocaine into the ACC, dHPC, or vHPC prior to retrieval to temporarily inactivate these structures. The results demonstrate that activity of the ACC and vHPC is required for the expression of a generalized fear memory, as inactivation of these regions returned the memory to a contextually precise form. Current theories of time-dependent generalization of contextual memories do not predict involvement of the vHPC. Our data suggest a novel role of this region in generalized memory, which should be incorporated into current theories of time-dependent memory generalization. We also show that the dorsal hippocampus plays a prolonged role in contextually precise memories. Our findings suggest a possible interaction between the ACC and vHPC controls the expression of fear generalization.
We recently proposed that retrograde amnesia does not result from a disruption of the consolidation/reconsolidation processes but rather to the integration of the internal state induced by the ...amnesic treatment within the initial memory. Accordingly, the performance disruption induced by an amnesic agent does not result from a disruption of the memory fixation process, but from a difference in the internal state present during the learning phase (or reactivation) and at the later retention test: a case of state-dependency. In the present article, we will review similarities and differences these two competing views may have on memory processing. We will also consider the consequences the integration concept may have on the way memory is built, maintained and retrieved, as well as future research perspectives that such a new view may generate.
Memory reactivation is an important process resulting from reexposure to salient training-related information whereby a memory is brought from an inactive to an active state. Reactivation is the ...first stage of memory retrieval but can result from the exposure to salient cues without any behavioral output. Such cue-induced reactivation, although frequently used by neuroscientists to study reconsolidation, has seldom been considered as a process in its own right and studied as such. This review presents arguments indicating that memory reactivation has two main consequences: (1) to enhance the accessibility of the target memory and (2) to make the memory malleable. Accordingly, reactivation creates a transient state during which the content of the memory is easily accessible and can be modified and/or updated. As both of these aspects can be observed shortly after memory reactivation, this review emphasizes that reconsolidation is not necessarily required for these processes and calls attention to reactivation as a factor in the dynamics of the memory.
Active (new and reactivated) memories are considered to be labile and sensitive to treatments disrupting the time-dependent consolidation/reconsolidation processes required for their stabilization. ...Active memories also allow the integration of new information for updating memories. Here, we investigate the possibility that, when active, the internal state provided by amnesic treatments is represented and integrated within the initial memory and that amnesia results from the absence of this state at testing. We showed in rats that the amnesia resulting from systemic, intracerebroventricular and intrahippocampal injections of the protein synthesis inhibitor cycloheximide, administered after inhibitory avoidance training or reactivation, can be reversed by a reminder, including re-administration of the same drug. Similar results were obtained with lithium chloride (LiCl), which does not affect protein synthesis, when delivered systemically after training or reactivation. However, LiCl can induce memory given that a conditioned taste aversion was obtained for a novel taste, presented just before conditioning or reactivation. These results indicate that memories can be established and maintained without de novo protein synthesis and that experimental amnesia may not result from a disruption of memory consolidation/reconsolidation. The findings more likely support the integration hypothesis: posttraining/postreactivation treatments induce an internal state, which becomes encoded with the memory, and should be present at the time of testing to ensure a successful retrieval. This integration concept includes most of the previous explanations of memory recovery after retrograde amnesia and critically challenges the traditional memory consolidation/reconsolidation hypothesis, providing a more dynamic and flexible view of memory.
This study provides evidence challenging the traditional consolidation/reconsolidation hypotheses that have dominated the literature over the past 50 years. Based on amnesia studies, that hypothesis states that active (i.e., new and reactivated) memories are similarly labile and (re)established in a time-dependent manner within the brain through processes that require de novo protein synthesis. Our data show that new/reactivated memories can be formed without protein synthesis and that amnesia can be induced by drugs that do not affect protein synthesis. We propose that amnesia results from memory integration of the internal state produced by the drug that is subsequently necessary for retrieval of the memory. This interpretation gives a dynamic view of memory, rapidly stored and easily updated when active.
False Memory in Nonhuman Animals Millin, Paula M; Riccio, David C
Learning & memory (Cold Spring Harbor, N.Y.),
10/2019, Letnik:
26, Številka:
10
Journal Article
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This paper examines recent evidence from behavioral and neuroscience research with nonhuman animals that suggests the intriguing possibility that they, like their human counterparts, are vulnerable ...to creating false memories. Once considered a uniquely human memory phenomenon, the creation of false memories in lower animals can be seen especially readily in studies involving memory for source, or contextual attributes. Furthermore, evidence of "implanted" misinformation has also been obtained. Here, we review that research and consider its relevance to our empirical understanding of false memories, as well as speculate about its potential clinical implications for trauma memory.
In previous studies using male rodents, context change disrupted a fear response at a short, but not a long, retention interval. Here, we examined the effects of context changes on fear responses as ...a function of time in male and female rats. Males displayed context discrimination at all intervals, whereas females exhibited generalization by 5 d. Ovariectomized females with no hormone replacement displayed context discrimination at 5 d, whereas those receiving 17ß-estradiol generalized their fear response to a neutral context. These results demonstrate that fear generalization for contextual cues occurs faster in female rats and is mediated, in part, by estrogens.
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