The standard model of memory consolidation versus the multiple trace theory two divergent views of the same process

In the so-called standard model of memory consolidation (Fig. 2), the hippocampus is believed to rapidly integrate and bind together information transmitted from distributed cortical networks that support the various features of a whole experience in order to form a coherent memory trace. Consolidation of this new memory trace at the cortical level would then occur slowly via repeated reactivation of hippocampal-cortical networksr to progressively increase the strength and stability of cortical-cortical connections. Over time, as memories mature, the role of the hippocampus would gradually diminish, leaving extrahippocampal regions, presumably cortical areas, to become in

Cortical modules

Fig. 2. The standard model of memory consolidation. Perceptual, motor and cognitive information is initially processed by several specializedprimary and associative cortical areas represented by cortical modules. The medial temporal lobe, including the hippocampus and related structures, integrates the various features of an experience and fuses them rapidly into a coherent memory trace. System consolidation then occurs slowly over time and involves a hippocampal-cortical dialogue to gradually strengthen cortical-cortical connections. This process involves not only the strengthening of existing cortical-cortical connections but also the creation of new connections between previously unconnected neurons via repeated activation of hippocampal-cortical networks during periods of quiet wakefulness or sleep. As cortical memories mature and acquire stability, the functional role of the hippocampus gradually diminishes, enabling structured cortical networks to ensure retrieval of remote memories independently. A key feature of this model is that changes in the strength of hippocampal-cortical connections are fast but short-lasting whereas changes within cortical-cortical connections are slow but long-lasting. (Adapted from Frankland and Bontempi 2005)

Fig. 2. The standard model of memory consolidation. Perceptual, motor and cognitive information is initially processed by several specializedprimary and associative cortical areas represented by cortical modules. The medial temporal lobe, including the hippocampus and related structures, integrates the various features of an experience and fuses them rapidly into a coherent memory trace. System consolidation then occurs slowly over time and involves a hippocampal-cortical dialogue to gradually strengthen cortical-cortical connections. This process involves not only the strengthening of existing cortical-cortical connections but also the creation of new connections between previously unconnected neurons via repeated activation of hippocampal-cortical networks during periods of quiet wakefulness or sleep. As cortical memories mature and acquire stability, the functional role of the hippocampus gradually diminishes, enabling structured cortical networks to ensure retrieval of remote memories independently. A key feature of this model is that changes in the strength of hippocampal-cortical connections are fast but short-lasting whereas changes within cortical-cortical connections are slow but long-lasting. (Adapted from Frankland and Bontempi 2005)

dependently capable of sustaining permanent memories and mediate their retrieval (Squire and Alvarez 1995; McClelland et al. 1995).

An alternative and challenging view is offered by the multiple trace theory, which posits that the hippocampus retains a permanent role in memory storage and retrieval as long as memories exist (Nadel and Moscovitch 1997). This view is supported by three main lines of clinical and experimental observations that cannot be accounted for by the standard model of memory consolidation. First, retrograde amnesia can, in some cases, be ungraded (i.e., 'flat'), wherein both recent and remote memories have been reported to be similarly impaired (Cipolotti et al. 2001). Second, certain retrograde amnesia gradients have been reported to last for decades or up to almost the entire human life span in some amnesic patients, thus raising the question of the ethological value of such an extended period of consolidation. Third, the observation of a retrograde amnesia gradient and its temporal extent may depend on the type of declarative memory to be consolidated (episodic, semantic or spatial; Moscovitch et al. 2006). The main features of the multiple trace theory are as follows. Each consciously experienced event would consist of a cohesive hippocampal-cortical ensemble. Each time that this particular event is recalled, it would be recreated and recoded in the form of multiple and stronger related memory traces dispersed over larger areas of hippocampal-cortical networks. Therefore, the relative sparing of remote memories in amnesic patients would be a function of the extent of hippocampal damage, with limited damage producing temporally graded retrograde amnesia and extensive lesions, resulting in a flat gradient for retrograde amnesia. Nadel and Moscovitch (1997, but for review, see also Moscovitch et al. 2006) further posit that the recurrent creation of multiple hippocampal-cortical traces would predominantly favor the integration of information with preexisting knowledge to form old semantic memories (memory for general knowledge of facts) whose retrieval could possibly occur without the contribution of the medial temporal lobe memory system. However, in the case of remotely acquired episodic memories, which are autobiographical and richly detailed in nature, these authors postulated that retrieval would always require the contribution of hippocampal-cortical networks.

It must be noted that the results of some case studies, for instance, patient E.P., who suffered large lesions of the medial temporal lobe following an episode of viral encephalitis, do not support the multiple trace theory (Teng and Squire 1999). Despite extensive hippocampal damage, this patient had excellent autobiographical memories from his youth and could accurately recall the spatial layout of the area where he grew up more than 50 years earlier. Even more astonishing was the ability of E.P. to mentally navigate and construct novel spatial routes to access specific locations of his past neighborhood, thus pointing to the existence of extrahippocampal spatial maps acquired long ago. In accordance with this case study, temporal gradients have been reported in animals even after complete hippocampal lesions. These discrepancies, especially the issue as to whether recalled memories in hippocampal patients such as E.P. or K.C. (Rosenbaum et al. 2000) are as vivid and richly detailed as in healthy patients, continue to be hotly debated (Bayley et al. 2003; Squire et al. 2004; Moscovitch et al. 2006).

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