Chapter 4: Concluding Remarks and Future Directions 131
4.3 Memory Organization – Our Understanding to Date 134
4.3.3 Memory Representations Across Time 139
Once acquired, long-term declarative memory is not static. It continues to evolve via integrative consolidation with existing memory, potentially with concurrent time-dependent changes in the underlying functional neuroanatomy. The primary evidence for the time- dependent process of memory consolidation comes from the pattern of memory impairment observed in temporally graded retrograde amnesia, which typically accompanies hippocampal anterograde amnesia. In temporally graded retrograde amnesia, recent episodic memory, i.e. those closer in time to the MTL insult, are compromised to a greater extent than remote memory. Memory impairments, both anterograde and retrograde, are typically more
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pronounced when damage extends beyond the hippocampus proper to the surrounding MTL structures such as the parahippocamal gyrus (Mishkin et al., 1998; Shimamura & Squire, 1987; Verfaellie et al., 2000). Observations of retrograde amnesia, particularly the relative sparing of remote memory, led to the hypothesis that, once outside a given time window, memory
retrieval is progressively less dependent on the hippocampus (Atir-Sharon et al., 2015; Ghosh & Gilboa, 2014; Takashima et al., 2006; van Kesteren et al., 2012). This change is thought to be due to the migration of memory representations to neocortical areas such as the medial prefrontal cortex and anterior temporal lobe, in a time-dependent, memory consolidation process (McClelland et al., 1995; Nadel & Moscovitch, 1997). In a manner that varies with the extent of hippocampal damage, the time span covering retrograde amnesia, and by extension, the memory consolidation process can last from a month to over 15 years in the most severe cases (McClelland et al., 1995)). Given their associations with semantic processing in healthy brains (Donaldson, Petersen, & Buckner, 2001; Gold et al., 2006; McDermott, Petersen, Watson, & Ojemann, 2003; A D Wagner et al., 2001), and the selective semantic impairments that result from their damage (Dronkers et al., 2004; Graham, Simons, Pratt, Patterson, & Hodges, 2000; Hart & Gordon, 1990; Holdstock et al., 2002; Turken & Dronkers, 2011), regions in the lateral temporal lobes, such as left MTG and ATL are proposed as candidates for consolidated neocortical memory representations (L. R. Squire & Wixted, 2011).
Based on the aforementioned observations, two prominent computational models have been constructed to explain the functional neuroanatomy supporting declarative memory acquisition and consolidation. The first is the Complementary Learning Systems (CLS)
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account (McClelland et al., 1995). The CLS model, which notably makes no explicit distinctions between semantic and episodic memory, posits that memory is first stored via hippocampal synaptic changes, which support reinstatement of a recent similar memory in the neocortex. Each reinstatement of a memory that is similar to a prior instance leads to slow, incremental changes in neocortical representations, to permit the neocortex to learn the common structure among the different instances. The hippocampal system permits rapid learning of novel information without disrupting existing memory in the neocortex.
Consolidation of novel information with existing memory in the neocortex occurs via slow incremental changes, ensuring remote memory stability in the face of novel memory acquisition.
The second model is the Multiple Traces Model (MTM) proposed by Nadel and Moscovich (Nadel & Moscovitch, 1997). As motivation for the model, Nadel and Moscovich point out that not all cases of retrograde amnesia are temporally graded. Episodic
(autobiographical) memory shows a shallow temporal gradient such that following
hippocampal damage, even the most remote episodic memory is impaired, whereas semantic memory (e.g. names of public figures) show a steeper temporal gradient. The two models are similar in that they both regard the hippocampus as central to rapid episodic memory
acquisition and both models generally regard neocortical memory consolidation as a relatively slower process. What sets the two models apart is that in the CLS model, the hippocampus is only prominently involved during retrieval and consolidation of recent, i.e. relatively novel memory. For remote memory matching a neocortical representation, the prefrontal cortex
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inhibits the hippocampus to avoid duplicate encoding (Frankland & Bontempi, 2005). On the other hand, in the MTM the hippocampus continues to be involved in the retrieval and reconsolidation of even remote memory. Reinstatement of a prior memory, or a slight variant thereof, creates a duplicate trace in the hippocampus. The common features present across multiple, slightly different memory traces can then be extracted to form what essentially becomes a decontextualized semantic memory. To explain temporally graded retrograde amnesia, the model posits that, because remote memory have likely been copied multiple times, they are more resistant to degradation due to hippocampal damage relative to recent memory.
As will be elaborated in greater detail below, the above discussion is particularly relevant here because one of the regions that we ascribed a role in memory retrieval of both previously known and newly learned words is in the parahippocampal gyrus, as opposed to canonical neocortical semantic regions in the temporal lobe (e.g. MTG). Given the above controversy in the literature regarding the involvement of MTL structures in semantic memory processes, this finding complements the literature by contributing evidence to the ongoing discussion from a sparsely documented adult word learning perspective. Another issue worth briefly mentioning regards the proposed slow nature of memory consolidation from initial MTL-dependent to subsequent neocortical representations. Given that the newly acquired words in the experiment failed to engage expected neocortical regions in the temporal lobe (e.g. MTG, ATL), subsequent discussions will draw on slow neocortical memory consolidation processes as a potential explanation.
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