Remote Memory Recall Research Articles

Hippocampal memory consolidation during sleep: a comparison of mammals and birds

The transition from wakefulness to sleep is marked by pronounced changes in brain activity. The brain rhythms that characterize the two main types of mammalian sleep, slow-wave sleep (SWS) and rapid eye movement (REM) sleep, are thought to be involved in the functions of sleep. In particular, recent theories suggest that the synchronous slow-oscillation of neocortical neuronal membrane potentials, the defining feature of SWS, is involved in processing information acquired during wakefulness. According to the Standard Model of memory consolidation, during wakefulness the hippocampus receives input from neocortical regions involved in the initial encoding of an experience and binds this information into a coherent memory trace that is then transferred to the neocortex during SWS where it is stored and integrated within preexisting memory traces. Evidence suggests that this process selectively involves direct connections from the hippocampus to the prefrontal cortex (PFC), a multimodal, high-order association region implicated in coordinating the storage and recall of remote memories in the neocortex. The slow-oscillation is thought to orchestrate the transfer of information from the hippocampus by temporally coupling hippocampal sharp-wave/ripples (SWRs) and thalamocortical spindles. SWRs are synchronous bursts of hippocampal activity, during which waking neuronal firing patterns are reactivated in the hippocampus and neocortex in a coordinated manner. Thalamocortical spindles are brief 7-14 Hz oscillations that may facilitate the encoding of information reactivated during SWRs. By temporally coupling the readout of information from the hippocampus with conditions conducive to encoding in the neocortex, the slow-oscillation is thought to mediate the transfer of information from the hippocampus to the neocortex. Although several lines of evidence are consistent with this function for mammalian SWS, it is unclear whether SWS serves a similar function in birds, the only taxonomic group other than mammals to exhibit SWS and REM sleep. Based on our review of research on avian sleep, neuroanatomy, and memory, although involved in some forms of memory consolidation, avian sleep does not appear to be involved in transferring hippocampal memories to other brain regions. Despite exhibiting the slow-oscillation, SWRs and spindles have not been found in birds. Moreover, although birds independently evolved a brain region--the caudolateral nidopallium (NCL)--involved in performing high-order cognitive functions similar to those performed by the PFC, direct connections between the NCL and hippocampus have not been found in birds, and evidence for the transfer of information from the hippocampus to the NCL or other extra-hippocampal regions is lacking. Although based on the absence of evidence for various traits, collectively, these findings suggest that unlike mammalian SWS, avian SWS may not be involved in transferring memories from the hippocampus. Furthermore, it suggests that the slow-oscillation, the defining feature of mammalian and avian SWS, may serve a more general function independent of that related to coordinating the transfer of information from the hippocampus to the PFC in mammals. Given that SWS is homeostatically regulated (a process intimately related to the slow-oscillation) in mammals and birds, functional hypotheses linked to this process may apply to both taxonomic groups.

Recent and remote memory recalls modulate different sets of stereotypical interlaminar correlations in Arc/Arg3.1 mRNA expression in cortical areas

Detailed organization of interlaminar relations in neuronal activity underlying recent and remote memory recall is unknown but essential for deciphering interlaminar connections involved in systems-level memory consolidation and permanent information storage. We mapped Arc/Arg3.1 (Arc) mRNA expression, a neuronal activity marker, at multiple rostro-caudal levels of the brain in Wistar rats following a platform search in a water-maze task. Strength of interlaminar correlations in Arc expression and modulation of the strength by memory recall in sensory, motor and association cortical areas were measured at 24 h and 1 month in memory retention. In order to estimate the extent of modular organization in neocortical function underlying memory recall, we studied multiple profiles of interlaminar coupling. At the level of cortical areas, we captured two robust stereotypical laminar patterns for distribution of strong and weak interlaminar correlations. These patterns emerged during both control swimming and navigation, at both retention delays. Within limits of these patterns, we established task-, time- and area-dependent modulations of the Arc correlations. Relative to swimming control, during memory recall, changes in strength of analogous interlaminar relations occurred largely in parallel but recent and remote recall modulated mostly distinct correlations. An effective remote memory recall was accompanied by fewer strengthened correlations as compared to recent recall. Thus, a behavioral experience is accompanied by a well-ordered or stereotypical spatial organization of interlaminar relations in neuronal activity distribution. Interlaminar correlations in Arc expression modulated by recent and remote memory recall could guide future inactivation and detection studies necessary to decipher interlaminar connections involved in systems-level consolidation and to reveal mnemonic plasticity specific to spatial memory.

Arc/Arg3.1 mRNA global expression patterns elicited by memory recall in cerebral cortex differ for remote versus recent spatial memories

The neocortex plays a critical role in the gradual formation and storage of remote declarative memories. Because the circuitry mechanisms of systems-level consolidation are not well understood, the precise cortical sites for memory storage and the nature of enduring memory correlates (mnemonic plasticity) are largely unknown. Detailed maps of neuronal activity underlying recent and remote memory recall highlight brain regions that participate in systems consolidation and constitute putative storage sites, and thus may facilitate detection of mnemonic plasticity. To localize cortical regions involved in the recall of a spatial memory task, we trained rats in a water-maze and then mapped mRNA expression patterns of a neuronal activity marker Arc/Arg3.1 (Arc) upon recall of recent (24 h after training) or remote (1 month after training) memories and compared them with swimming and naive controls. Arc gene expression was significantly more robust 24 h after training compared to 1 month after training. Arc expression diminished in the parietal, cingulate and visual areas, but select segments in the prefrontal, retrosplenial, somatosensory and motor cortical showed similar robust increases in the Arc expression. When Arc expression was compared across select segments of sensory, motor and associative regions within recent and remote memory groups, the overall magnitude and cortical laminar patterns of task-specific Arc expression were similar (stereotypical). Arc mRNA fractions expressed in the upper cortical layers (2/3, 4) increased after both recent and remote recall, while layer 6 fractions decreased only after the recent recall. The data suggest that robust recall of remote memory requires an overall smaller increase in neuronal activity within fewer cortical segments. This activity trend highlights the difficulty in detecting the storage sites and plasticity underlying remote memory. Application of the Arc maps may ameliorate this difficulty.

Impairment of episodic and semantic autobiographical memory in patients with mild cognitive impairment and early Alzheimer's disease

Autobiographical memory includes the retrieval of personal semantic data and the remembrance of incident or episodic memories. In retrograde amnesias, it has been observed that recall of autobiographical memories of recent events is poorer than recall of remote memories. Alzheimer's disease (AD) may also be associated with a temporal gradient (TG) in memory decline, though studies have yielded inconsistent results on this point. They have also yielded inconsistent results on whether AD might differentially affect semantic and episodic remembrance. Here, we compared autobiographical memory of childhood, early adulthood, and recent life among healthy control (HC) subjects, patients with early AD, and patients with amnesic mild cognitive impairment (aMCI). Both the aMCI and AD patients exhibited declines in recall of autobiographical incidents and semantic information. In AD patients, both components of autobiographical memory had a clear TG, with better preservation of memories of childhood than those of early adulthood and recent life. The TG of autobiographical memory decline in AD patients is more compatible with the Cortical Reallocation Theory than with the Multiple Trace Theory of memory consolidation. In contrast to AD patients, aMCI patients exhibited impaired recall of personal facts and autobiographical incidents relating only to recent life. The significant decline in autobiographical memory for recent life that occurred in aMCI patients suggests that deterioration of consolidation of personal facts and events begins with commencement of functional impairment in the hippocampus.

Medial Temporal Lobe Activity during Retrieval of Semantic Memory Is Related to the Age of the Memory

We measured brain activity using event-related fMRI as participants recalled answers to 160 questions about news events that had occurred during the past 30 years. Guided by earlier findings from patients with damage limited to the hippocampus who were given the same test material, we looked for regions that exhibited gradually decreasing activity as participants recalled memories from 1-12 years ago and a constant level of activity during recall of more remote memories. Regions in the medial temporal lobe exhibited a decrease in brain activity in relation to the age of the memory (hippocampus, temporopolar cortex, and amygdala). Regions in the frontal lobe, temporal lobe, and parietal lobe exhibited the opposite pattern. The findings for all of these regions were unrelated to the richness of the memories, to how well test questions were remembered later (encoding for subsequent memory), nor to how frequently semantic memories were accompanied by personal, episodic recollections. Last, activity in a different group of regions (perirhinal cortex, parahippocampal cortex, and inferior temporal gyrus) was associated with how well the test questions were subsequently remembered. The results support the idea that medial temporal lobe structures play a time-limited role in semantic memory.

Recall of remote episodic memories can appear deficient because of a gist-based retrieval orientation

Determining whether patients with amnesia can succeed in remembering their distant past has pivotal implications for theories of memory storage. However, various factors influence recall. We speculated that some patients with anterograde amnesia adopt a gist-based retrieval orientation for memories from all time periods, thereby exaggerating remote recall deficits. We tested whether an experimentally induced gist-based retrieval orientation could indeed hinder remote recall. Healthy individuals described photographs of complex scenes (e.g., of a cluttered desk) either with many words or few words (detail- or gist-based manipulation, respectively). They subsequently recalled autobiographical events and produced less episodic information after engaging the gist-based compared to the detail-based orientation. These results demonstrate the ease with which a gist-based orientation can produce apparent recall impairments. Deficits in remote episodic recall, and in future-event imagining, must thus be interpreted in light of habitual tendencies toward gist-based retrieval that some amnesic patients may exhibit.

Reorganization of learning-associated prefrontal synaptic plasticity between the recall of recent and remote fear extinction memory

We have previously shown that fear extinction is accompanied by an increase of synaptic efficacy in inputs from the ventral hippocampus (vHPC) and mediodorsal thalamus (MD) to the medial prefrontal cortex (mPFC) and that disrupting these changes to mPFC synaptic transmission compromises extinction processes. The aim of this study was to examine whether these extinction-related changes undergo further plasticity as the memory of extinction becomes more remote. Changes in synaptic efficacy in both vHPC-mPFC and MD-mPFC inputs were consequently analyzed when the memory was either 1 d or 7 d old. Increases of synaptic efficacy in the vHPC-mPFC pathway were observed when the memory was 1 d old, but not 7 d after initial extinction. In contrast, potentiation of synaptic efficacy in the MD-mPFC pathway increased over time. In rats that received low-frequency vHPC stimulation immediately after extinction, both vHPC-mPFC and MD-mPFC inputs failed to develop potentiation, and the recall of extinction (both recent and remote memories) was impaired. These findings suggest that post-extinction potentiation in vHPC-mPFC inputs may be necessary for both the recall of recent memory and post-extinction potentiation in the MD-mPFC inputs. This late potentiation process may be required for the recall of remote extinction memory.

Stability of recent and remote contextual fear memory

Following initial encoding, memories undergo a prolonged period of reorganization. While such reorganization may occur in many different memory systems, its purpose is not clear. Previously, we have shown that recall of recent contextual fear memories engages the dorsal hippocampus (dHPC). In contrast, recall of remote contextual fear memories engages a number of different cortical regions, including the anterior cingulate cortex (ACC). To examine whether this reorganization leads to greater memory stability, we examined reconsolidation of 1 d-old (recent) and 36 d-old (remote) contextual fear memory in mice. We infused the protein synthesis inhibitor, anisomycin (ANI), into either the dHPC or ACC immediately following retrieval of either a recent or remote contextual fear memory. In the dHPC, ANI infusions disrupted subsequent expression of recent, but not remote, contextual fear memory. Similar infusions into the ACC had no effect on either recent or remote contextual fear memories, whereas systemically applied ANI blocked subsequent remote memory expression when long re-exposure durations were used. Together, these data suggest that as memories mature they become increasingly stable. Furthermore, the dissociation between the effects of systemically and centrally administered ANI on remote memory suggests that stability is due, in part, to the distributed nature of remote contextual fear memories.

A role for the prefrontal cortex in recall of recent and remote memories

Declarative memories are thought to be initially stored in the hippocampus, and then transferred to the neocortex. This is a key feature of the standard model of consolidation and is supported by studies reporting a requirement for activity within the neocortex for recall of remote, but not recent, hippocampal-dependent memories. New evidence from our and other laboratories, however, suggests that, for trace fear conditioning, memories are stored in the rodent medial prefrontal cortex and in the hippocampus from the time of training. Consistent with this, we show that activity in the medial prefrontal cortex is necessary for retrieval of recent and remote memories, suggesting that information stored in this neocortical structure from the time of training is necessary for memory recall.

Fast track to the medial prefrontal cortex

Studies of brain-damaged patients have provided remarkable insights into how our memories are organized (1). In particular, these studies have established that memory consolidation is a dynamic process involving gradual (but quite dramatic) reorganization of the circuits supporting memory over time (2, 3). A pioneer in this field was the French psychologist Theodule Ribot. In the late part of the 19th century, Ribot described how memory loss after brain insult tended to be related to the age of the memory: the effect on more recent memories was typically greater than that on older (or more remote) memories (4). Later studies established that damage to the medial temporal lobe (5), and more specifically the hippocampus (1), is responsible for this typical graded amnesia. This Ribot gradient has suggested that the hippocampus is only temporarily involved in the storage and recall of certain types of memory, and that these functions must be subsumed by extrahippocampal structures as memories mature (2, 6). Hippocampal damage in experimental animals also preferentially disrupts recent memory. Such examples, from mice to monkeys, suggest that time-dependent memory reorganization is an evolutionarily conserved process for memory consolidation (3). However, differences do exist between human and experimental animal studies, and these differences have made it difficult to come up with a unified mechanistic account of memory consolidation. For example, the lengths of the gradients vary dramatically from days or weeks (for example, in rodents) to years (in humans), suggesting that the rate of reorganization may vary greatly across species. Second, although studies in experimental animals have begun to successfully identify extrahippocampal brain regions that support remote memory recall, the evidence from human studies of remote memory has been much less consistent, and it has even been suggested that autobiographical memories may never become truly independent of the …

Recall of remote episodic memory in amnesia

Recall of remote episodic memory was assessed in three types of amnesic patient whose remote semantic memory had been evaluated previously. Patients with Korsakoffs syndrome, case N.A. and patients receiving electroconvulsive therapy all succeeded in recalling specific autobiographical episodes in response to single-word cues, and in many conditions performed as well as control subjects. Their pattern of performance generally paralleled that obtained in previous tests of remote semantic memory. These results argue against a view that amnesia reflects a selective deficit of episodic memory and suggest that the semantic-episodic distinction cannot illuminate the fundamental deficit in amnesia. Nor can the facts of amnesia confirm or deny the validity of this distinction in normal memory.

Transient global amnesia due to arterial embolism.

Transient global amnesia is a well-recognized clinical entity, but its pathophysiology has remained obscure. Two typical cases with onset during cardiac angiography have been observed in which arterial embolization appears to have been the cause of this syndrome. Both patients had the sudden onset of a profound global recent memory defect with sparing of immediate recall and relative sparing of remote memory except for a variable degree of retrograde amnesia. A detailed neurological examination failed to reveal any additional central nervous system dysfunction at any time during the amnestic episode. Complete recovery occurred except for a persistent amnesia for events occurring during the attack.