Hippocampal Complex Contribution to Retention and Retrieval of Recent and Remote Episodic and Semantic Memories: Evidence from Behavioral and Neuroimaging Studies of Healthy and Brain-Damaged People (original) (raw)
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Multiple trace theory of human memory: Computational, neuroimaging, and neuropsychological results
Hippocampus, 2000
Hippocampal-neocortical interactions in memory have typically been characterized within the ''standard model'' of memory consolidation. In this view, memory storage initially requires hippocampal linking of dispersed neocortical storage sites, but over time this need dissipates, and the hippocampal component is rendered unnecessary. This change in function over time is held to account for the retorgrade amnesia (RA) gradients often seen in patients with hippocampal damage. Recent evidence, however, calls this standard model into question, and we have recently proposed a new approach, the ''multiple memory trace'' (MMT) theory. In this view, hippocampal ensembles are always involved in storage and retrieval of episodic information, but semantic (gist) information can be established in neocortex, and will survive damage to the hippocampal system if enough time has elapsed. This approach accounts more readily for the very long RA gradients often observed in amnesia. We report the results of analytic and connectionist simulations that demonstrate the feasibility of MMT. We also report a neuroimaging study showing that retrieval of very remote (25-year-old) memories elicits as much activation in hippocampus as retrieval of quite recent memories. Finally, we report new data from the study of patients with temporal lobe damage, using more sensitive measures than previously the case, showing that deficits in both episodic and spatial detail can bed observed even for very remote memories. Overall, these findings indicate that the standard model of memory consolidation, which views the hippocampus as having only a temporary role in memory, is wrong. Instead, the data support the view that for episodic and spatial detail the hippocampal system is always necessary. Hippocampus 2000;10:352-368.
The Hippocampus Remains Activated over the Long Term for the Retrieval of Truly Episodic Memories
PloS one, 2012
The role of the hippocampus in declarative memory consolidation is a matter of intense debate. We investigated the neural substrates of memory retrieval for recent and remote information using functional magnetic resonance imaging (fMRI). 18 young, healthy participants learned a series of pictures. Then, during two fMRI recognition sessions, 3 days and 3 months later, they had to determine whether they recognized or not each picture using the “Remember/Know” procedure. Presentation of the same learned images at both delays allowed us to track the evolution of memories and distinguish consistently episodic memories from those that were initially episodic and then became familiar or semantic over time and were retrieved without any contextual detail. Hippocampal activation decreased over time for initially episodic, later semantic memories, but remained stable for consistently episodic ones, at least in its posterior part. For both types of memories, neocortical activations were observed at both delays, notably in the ventromedial prefrontal and anterior cingulate cortices. These activations may reflect a gradual reorganization of memory traces within neural networks. Our data indicate maintenance and strengthening of hippocampal and cortico-cortical connections in the consolidation and retrieval of episodic memories over time, in line with the Multiple Trace theory (Nadel and Moscovitch, 1997). At variance, memories becoming semantic over time consolidate through strengthening of cortico-cortical connections and progressive disengagement of the hippocampus.
Neural Plasticity, 2007
Multiple trace theory (MTT) predicts that hippocampal memory traces expand and strengthen as a function of repeated memory retrievals. We tested this hypothesis utilizing fMRI, comparing the effect of memory retrieval versus the mere passage of time on hippocampal activation. While undergoing fMRI scanning, participants retrieved remote autobiographical memories that had been previously retrieved either one month earlier, two days earlier, or multiple times during the preceding month. Behavioral analyses revealed that the number and consistency of memory details retrieved increased with multiple retrievals but not with the passage of time. While all three retrieval conditions activated a similar set of brain regions normally associated with autobiographical memory retrieval including medial temporal lobe structures, hippocampal activation did not change as a function of either multiple retrievals or the passage of time. However, activation in other brain regions, including the precu...
Memory function and the hippocampus
Frontiers of neurology and neuroscience, 2014
There has been a long tradition in memory research of adopting the view of a vital role of the medial temporal lobe and especially the hippocampus in declarative memory. Despite the broad support for this notion, there is an ongoing debate about what computations are performed by the different substructures. The present chapter summarizes several accounts of hippocampal functions in terms of the cognitive processes subserved by these structures, the information processed, and the underlying neural operations. Firstly, the value of the distinction between recollection and familiarity for the understanding of the role the hippocampus plays in memory is discussed. Then multiple lines of evidence for the role of the hippocampus in memory are considered. Cumulating evidence suggests that the hippocampus fosters the binding of disparate cortical representations of items and their spatiotemporal context into a coherent representation by means of a sparse conjunctive neural coding. This ass...
Hippocampus, 2001
It has been argued that the role of the hippocampus in memory is time-limited: during a period of memory consolidation, other brain regions such as the neocortex are said to acquire the ability to support memory retention and retrieval on their own. An alternative view is that retention and retrieval of memory for autobiographical episodes depend on the hippocampal complex, regardless of the age of the memory. We examined the participation of the hippocampal complex in a functional magnetic resonance imaging (fMRI) study in which participants were asked to recollect autobiographical events that occurred either within the last 4 years or more than 20 years ago. We found equivalent levels of hippocampal activation in both conditions in all participants (N ؍ 10). In addition, activation in neocortical regions did not differ as a function of the age of the memory, even though most of the recent memories recalled were less than 2 years old and the remote memories more than 35 years old. The results support the notion that the hippocampal complex participates in retention and recovery of even very old autobiographical memories, and place boundary conditions on theories of memory consolidation. Hippocampus 2001;11:707-714.
Re-experiencing old memories via hippocampus: a PET study of autobiographical memory
Neuroimage, 2004
The time-scale of medial temporal lobe (MTL) involvement in storage and retrieval of episodic memory is keenly debated. To test competitive theories of long-term memory consolidation, the present work aimed at characterizing which cerebral regions are involved during retrieval of recent and remote strictly episodic autobiographical memory. Using positron emission tomography (PET), we examined mental retrieval of recent (0 -1 year) and remote (5 -10 years) autobiographical memories, controlling for the nature of the autobiographical memories (i.e., specificity, state of consciousness, vividness of mental visual imagery, emotion) retrieved during scanning by behavioral measures assessed at debriefing for each event recalled. Cognitive results showed that specificity and emotion did not change with time interval although both autonoetic consciousness and mental image quality were significantly higher for recent memories, suggesting an underlying shift in the phenomenal experience of remembering with the passage of time. The SPM analysis revealed common activations during the recollection of recent and remote memories that involved a widespread but mainly left-sided cerebral network, consistent with previous studies. Subtraction analysis demonstrated that the retrieval of recent (relative to remote) autobiographical memories principally activated the left dorsolateral prefrontal cortex whereas the retrieval of remote (relative to recent) autobiographical memories activated the inferior parietal cortex bilaterally. ROIs analysis revealed more hippocampal activity for remote memories than for recent ones and a preferentially rightsided involvement of the hippocampal responses whatever the remoteness of autobiographical memories. New insights based on higher hippocampal response to the remoteness of episodic autobiographical memories challenge the standard model and are less discrepant with the multiple trace theory. D
The cognitive neuroscience of remote episodic, semantic and spatial memory
Current Opinion in Neurobiology, 2006
The processes and mechanisms implicated in retention and retrieval of memories as they age is an enduring problem in cognitive neuroscience. Research from lesion and functional neuroimaging studies on remote episodic, semantic and spatial memory in humans is crucial for evaluating three theories of hippocampal and/or medial temporal lobeneocortical interaction in memory retention and retrieval: cognitive map theory, standard consolidation theory and multiple trace theory. Each theory makes different predictions regarding first, the severity and extent of retrograde amnesia following lesions to some or all of the structures mentioned; second, the extent of activation of these structures to retrieval of memory across time; and third, the type of memory being retrieved. Each of these theories has strengths and weaknesses, and there are various unresolved issues. We propose a unified account based on multiple trace theory. This theory states that the hippocampus is needed for re-experiencing detailed episodic and spatial memories no matter how old they are, and that it contributes to the formation and assimilation of semantic memories and schematic spatial maps.
Hippocampal Signatures of Episodic Memory: Evidence from Single-Unit Recording Studies
Frontiers in Behavioral Neuroscience, 2013
What hippocampal neural firing patterns signal memory and, more importantly, how is this memory code used by associated structures to translate a memory into a decision or action? Candidate hippocampal activity patterns will be discussed including (1) trajectoryspecific firing of place cells with place fields on an overlapping segment of two (or more) distinct trajectories (2) prospective firing of hippocampal neurons that signal an upcoming event or action, and (3) place cell remapping to changes in environment and task. To date, there has not been compelling evidence for any of these activity patterns being the neural substrate of episodic memory. New findings suggest that learning and memory processes are emergent properties of interregional interactions and not localized within any one discrete brain region. Therefore, the next step in understanding how remapping and trajectory coding participate in memory coding may be to investigate how these activity patterns relate to activity in anatomically connected structures such as the prefrontal cortex.