Forgetting as a function of interference, inhibition, and decay

1.4.1. Forgetting due to interference and inhibition

Following memory acquisition, representations are prone to forgetting. Historically, the prevailing assumption of forgetting was that encoding of new information can disrupt or be disrupted by an existing memory representation (see Wixted, 2004 for review). For instance, Jenkins and Dallenbach (1924) demonstrated that retention for nonsense syllables was increased in participants who slept between encoding and retrieval, relative to those who remained awake. As participants who remained awake were expected to be exposed to more interfering material following encoding, the finding that sleep reduced forgetting was taken to suggest that new memory formation throughout the day, in participants who remained awake, retroactively interfered with the critical test information. However, Underwood (1957) later argued that much of forgetting observed in previous experiments was accounted for by the material participants learnt prior, rather than after, the critical test information, suggesting that

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retention was at least as susceptible to proactive as retroactive interference (see Postman, 1971 for review).

More recently it has been argued that forgetting is not always a consequence of new or past learning per se, but can also be the result of inhibitory processes established during retrieval to overcome interference (Anderson, 2003). This proposal holds that when a situation demands the selective retrieval of a memory, inhibitory processes present at retrieval will lead to long-lasting decreases in retention for other memories that may compete or interfere with the

‘target’ memory (Anderson, 2003). This proposal is motivated by evidence presented by Anderson, Bjork, and Bjork (1994). Anderson et al. (1994) had participants learn six category exemplars of, for instance, fruits and asked participants to repeatedly retrieve three of the six exemplars in response to a cue exemplar stem (e.g., fruit: or_ for the exemplar orange).

Anderson et al. (1994) observed that not only did performance for the retrieved exemplars increase on a later memory test, but memory for non-retrieved exemplars (e.g., banana) decreased relative to a baseline category of exemplars. This phenomenon is referred to as

‘retrieval-induced forgetting’ (Anderson et al., 1994). Retrieval-induced forgetting appears to emerge as an effect of interference at retrieval, with greater decreases in memory performance seen for exemplars that show a greater amount of relatedness to the target memory (Anderson et al., 1994). This effect is not only seen for exemplars within the same category, but extends to exemplars that are from different categories but nevertheless relate to a ‘target’ memory (Anderson & Spellman, 1995), suggesting that the effect of repeated retrieval can generalise to any representation that interferes with a target memory.

The idea that retrieval-induced forgetting is related to inhibitory processes at retrieval is supported by neuroimaging work. For instance, Kuhl, Dudukovic, Kahn, and Wagner (2007) had participants learn a series of overlapping word pairs (e.g., attic-dust and attic-junk).

During retrieval practice, participants were repeatedly presented with a cue word and the first letter of the associated word required to be retrieved (e.g., attic-d___ for the associate dust).

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Kuhl et al. (2007) observed that activity in the prefrontal cortex – a region associated with inhibitory control processes (see Miller & Cohen, 2001 for review) – decreased across the first and final retrieval practice trial. The reduction in activity in the prefrontal cortex correlated with decreases in memory for the ‘unpractised’ association (i.e., attic-junk) on a final memory test, suggesting that inhibitory demands during retrieval practice decreased as the unpractised association was forgotten (see also Wimber, Rutschmann, Greenlee, & Bäuml, 2008). Further evidence for this was presented by Wimber, Alink, Charest, Kriegeskorte, and Anderson (2015). Wimber et al. (2015) had participants learn a series of overlapping associations (e.g., sand-Marilyn Monroe, sand-hat), and then asked participants to selectively retrieve one of the associative items (e.g., Marilyn Monroe), but not the other item (e.g., hat) in response to a retrieval cue (e.g., sand). During repeated retrievals, Wimber et al. (2015) observed that cortical activity patterns became more dissimilar to activity patterns associated with the unpractised item. This was taken as evidence that retrieval practice led to the ‘suppression’ of cortical representations of the unpractised item (Wimber et al., 2015). Consistent with this, the extent of this cortical suppression effect was shown to correlate with the forgetting of a non-practised item (e.g., hat) (but see Potter, Huszar, & Huber, 2018). This suppression effect was also shown to correlate with activity in the prefrontal cortex during retrieval practice, consistent with the proposal that inhibitory processes can lead to forgetting when two or more memory representations interfere with each other at retrieval (Anderson, 2003).

1.4.2. Forgetting as a function of decay

Interference from ongoing learning is not thought to be the primary mechanism for forgetting of memory representations supported by the hippocampus (Sadeh, Ozubko, Winocur, &

Moscovitch, 2014, 2016). As representations in the neocortex are overlapping in nature, information represented in the neocortex is likely to be susceptible to interference (McClelland et al., 1995; Norman & O’Reilly, 2003). However, the sparse activity patterns used by the hippocampus are thought to support pattern separation (Bakker et al., 2008; Berron et al.,

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2016). As such, memory representations in the hippocampus are less likely to interfere with each other (Yassa & Stark, 2011). Consistent with this, activity in the hippocampus during the repeated encoding of an A-C pair (e.g., watch-pipe) has been shown to support retention of a previously learnt, and overlapping A-B pair (e.g., watch-sink) (Kuhl, Shah, Dubrow, &

Wagner, 2010; see also Chanales, Dudukovic, Richter, & Kuhl, 2019), suggesting that activity in the hippocampus minimises the likelihood of forgetting due to interference during encoding.

Sadeh, Ozubko, Winocur, and Moscovitch (2014) proposed that differences in the mechanisms of forgetting may be reflected in the representations and/or retrieval processes that support memory. Specifically, Sadeh et al. (2014) suggested that familiarity - a process thought to be supported by the perirhinal cortex (Diana et al., 2007; Mayes et al., 2007) – is sensitive to forgetting via interference. However, because pattern separation in the hippocampus ensures that memory representations are less likely to interfere with each other (Yassa & Stark, 2011), recollection – a process thought to be supported by the hippocampus (Diana et al., 2007; Mayes et al., 2007; Yonelinas, 2002) – is more likely to be forgotten via decay (Sadeh et al., 2014).

Some support for this proposal comes from evidence showing that while memory for words judged as ‘remembered’ decreases between encoding and retrieval after a one week-delay, recognition for words judged as ‘known’ does not decrease as a function of delay (Gardiner &

Java, 1991; but see Hockley & Consoli, 1999). However, Sadeh, Ozubko, Winocur, and Moscovitch (2016) provided more direct evidence for this proposal by manipulating both the effect of interference and delay on retention for words judged as either recollected or familiar.

Sadeh et al. (2016) observed that while memory for words judged as familiar decreased predominately as an effect of interference (i.e., presenting participants with additional words following encoding), memory for words judged as recollected decreased as a function of the length of the delay between encoding and retrieval, irrespective of the degree of interference (consistent with forgetting via decay).

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The proposal by Sadeh et al. (2014) is motivated by previous work suggesting that the forgetting of hippocampal representations is the result of decay (Frankland, Kohler, &

Josselyn, 2013; Hardt, Nader, & Nadel, 2013); possibly due to ongoing neurogenesis in the hippocampus (Frankland et al., 2013) or more active regulatory processes during sleep that

‘remove’ hippocampal representations based on their behavioural relevance or representational strength (Hardt et al., 2013). The proposal that forgetting of hippocampal representations is the result of decay has some parallels with theories of systems consolidation (e.g., McClelland et al., 1995; Squire & Alvarez, 1995) in that it assumes that decay involves the gradual deterioration of a hippocampal representation, leaving only the neocortical components of the memory behind. Prior to consolidation, the decay of a hippocampal representation can leave neocortical representations prone to interference and lead to forgetting (Frankland et al., 2013; Hardt et al., 2013). However, for neocortical representations that have been sufficiently strengthened via consolidation, the consequence of decay in the hippocampus is thought to be limited to the loss of contextual information associated with a particular event (Hardt et al., 2013); consistent with the proposal that systems consolidation may be associated with a formation of a gist-like representation in the neocortex (Winocur &

Moscovitch, 2011). Thus, forgetting will reflect an interaction between two opposing processes, memory consolidation and memory decay (Frankland et al., 2013).

1.4.3. Summary

Research on forgetting has tended to focus on the effect of interference during learning (see Wixted, 2004 for review). Although it is accepted that some of forgetting will be due to interference, it has been argued that forgetting is not always due to interference during learning, but can also reflect inhibitory processes that are established to overcome interference at retrieval (Anderson, 2003). However, more recently it has been suggested that some of forgetting may also be due to memory decay (Frankland et al., 2013; Hardt et al., 2013; Sadeh et al., 2016). This proposal draws on our neuroscientific understanding of the anatomical

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characteristics that distinguish medial temporal lobe regions, such as the hippocampus, from extra-hippocampal regions and the neocortex more generally. Due to the presence of pattern separation in the hippocampus, the forgetting of representations, and/or retrieval processes, supported by the hippocampus is not thought to occur via interference. Instead, it has been proposed that forgetting of a hippocampal representation may be due to the decay of the underlying memory trace itself.