Multiple trace theory of human memory: Computational, neuroimaging, and neuropsychological results

Abstract

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 10:352–368, 2000 © 2000 Wiley‐Liss, Inc.

Consolidation of memory

“…As we have already argued above, this does not appear to be the case in the animal studies: remote memories retrieved in lesioned subjects are not the same as remote memories available to intact subjects. 3 Similar findings in human amnesics were reported recently (Viskontas et al, 2000;Westmacott and Moscovitch, 2000;Nadel et al, 2000) for tests of autobiographical memory. No matter how remote, memories retrieved by amnesic subjects are not qualitatively the same as those available to intact subjects.…”

“…Thus, remote spatial memories that can be retrieved are not qualitatively and quantitatively the same as those observed in control subjects. Much the same conclusion has been reached from a study of autobiographical memory in temporal lobe patients (Viskontas et al, 2000;Nadel et al, 2000): when increasingly sensitive measures are used, persistent deficits in remote memory are observed at all time points.…”

The rodent hippocampus and spatial memory: from synapses to systems

“…In support of the sematicization view of memory consolidation [392,393], it is sometimes observed that the remote autobiographical memories that survive in human temporal lobe amnesics are impoverished in detail and richness, and qualitatively different from those in neurologically intact subjects [for reviews, see refs. 390,391,394,395], but it is also possible that these impoverished details are a result of the extratemporal lobe damage that is present in these patients. Similar suggestions have been made with regard to spatial memory in rodents [344,390].…”

The COST of explicit memory

“…A neuropsychological study (Viskontas et al 2000) on patients who underwent a unilateral temporal lobectomy showed extensive RA back to childhood. Nadel et al (2000) also demonstrated that, in the model, the extent of the damage implies degrees of RA. Again, the Ribot curves are supported.…”