Short-Term Memory and Long-Term Memory are Still Different
Dennis Norris MRC Cognition and Brain Sciences Unit, Cambridge, United Kingdom
A commonly expressed view is that short-term memory (STM) is nothing more than activated long-term memory. If true, this would overturn a central tenet of cognitive psychology—the idea that there are functionally and neurobiologically distinct short- and long-term stores. Here I present an updated case for a separation between short- and long-term stores, focusing on the computational demands placed on any STM system. STM must support memory for previously unencountered information, the storage of multiple tokens of the same type, and variable binding. None of these can be achieved simply by activating long-term memory. For example, even a simple sequence of digits such as “1, 3, 1” where there are 2 tokens of the digit “1” cannot be stored in the correct order simply by activating the representations of the digits “1” and “3” in LTM. I also review recent neuroimaging data that has been presented as evidence that STM is activated LTM and show that these data are exactly what one would expect to see based on a conventional 2-store view.
Keywords: long-term memory, memory, STM, working memory
For more than a century most psychologists have accepted that there are distinct memory systems responsible for long and short- term storage. Originally based entirely on introspection (e.g., James, 1890), the idea that there are separate long- and short-term memory (LTM and STM, respectively) systems subsequently be- came a core assumption of modern cognitive psychology. From the 1960s most cognitive models of memory have assumed that there are separate stores (Atkinson & Shiffrin, 1968; Baddeley, 1986; Baddeley & Hitch, 1974; Brown, Preece, & Hulme, 2000; Burgess & Hitch, 1992, 2006; Lewandowsky & Farrell, 2000; Page & Norris, 1998a, 1998b, 2009; Waugh & Norman, 1965). This re- mains the framework guiding almost all cognitive work on verbal STM.
There are dissenting voices. A number of authors have argued that the behavioral data are more parsimoniously accounted for by assuming that there is only a single memory system responsible for both short- and long-term storage (Brown, Neath, & Chater, 2007; Cowan, 1988, 1999; Crowder, 1993; Crowder & Neath, 1991; Engle, Kane, & Tuholski, 1999; Gruneberg, 1970; Jonides et al., 2008; McElree, 2006; Melton, 1963; Nairne, 2002; Poirier & Saint-Aubin, 1996; Surprenant & Neath, 2009). Some have argued that STM is nothing more than activated LTM (Cowan, 1988, 1999; Oberauer, 2002, 2009). This conception of the relation between STM and LTM has become increasingly popular in neu-
roimaging research (Acheson, Hamidi, Binder, & Postle, 2011; Cameron, Haarmann, Grafman, & Ruchkin, 2005; D’Esposito & Postle, 2015; Jonides et al., 2008; LaRocque et al., 2015; Postle, 2006; Ranganath & Blumenfeld, 2005; Ruchkin, Grafman, Cam- eron, & Berndt, 2003). However, there have been no attempts to present an updated case for a multicomponent view of memory in which there is a clear theoretical and conceptual distinction be- tween LTM and short-term stores. Most of the papers cited above have taken a data-driven approach to the debate, in which involves cataloguing similarities between LTM and STM. Here I take a very different approach and consider the computational requirements of a system that could support retention of information over the short term. These impose strong constraints on the architectural rela- tionship between LTM and STM. The overall conclusion will be that, although LTM has an essential role to play, STM cannot be supported simply by activating LTM. Even simple tasks such as remembering a sequence of digits can only be performed by supplementing LTM with some additional mechanism. This addi- tional mechanism is not part of LTM, but has all of the properties typically ascribed to a separate short-term store. Although I will focus primarily on verbal STM, the underlying logic of the argu- ments applies equally well to STM in other domains. This article begins with a brief review of the core data supporting a distinction between long- and short-term stores. This is followed by an anal- ysis of cognitive theories that have proposed that STM is activated LTM. The concern here will be to establish exactly what the substantive claims of such theories are. I then review the neuro- imaging data that have been presented as support for the activation view. In the second half of the paper I focus on computational considerations that argue strongly against the idea that STM might be nothing more than activated LTM. The central problem for activation-based models is that STM has to be able to store arbitrary configurations of novel information. For example, we can remember novel sequences of words or dots in random positions on a screen. These cannot possibly have preexisting representa- tions in LTM that could be activated. The digit sequence 133646
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might activate LTM representations of the digits 1, 3, 6 and 4, but some extra mechanism is required to encode the order of the digits and the fact that there are two tokens of the digits 3 and 6. Activating the LTM representations of 1, 3, 6 and 4 is not enough. STM can also store more complex structural representations to encode novel objects and the relation between them. Any viable model of STM must therefore be endowed with additional pro- cesses beyond simple activation of LTM. At the very least there must be a mechanism capable of storing multiple tokens, recalling those tokens in the correct order, and creating novel structured representations that cannot yet be in LTM.
I will also ask what it is that we actually store in STM. Does STM contain copies of representations or pointers to representa- tions? If STM contains pointers, do those pointers address LTM, or might those pointers address representations held within the short- term storage system itself? I suggest that, at some level, STM must make use of pointers, but that there are strong computational advantages to having pointers operate within the bounds of a modality-specific STS such as the phonological store component of Baddeley and Hitch’s (1974) Working Memory model. That is, consideration of how a pointer-based system might work provides further support for the idea that there must be a functional distinc- tion between short- and long-term stores.
The idea that STM is merely activated LTM is usually pitted against the classic idea that STM consists of a buffer (or buffers) that holds copies of the items in memory. This view of memory is implicit in Atkinson and Shiffrin’s (1966, 1968, 1971) modal model. Their, 1971 paper begins: “Memory has two components: short-term and long-term” (p. 3). The Atkinson and Shiffrin model is shown in Figure 1A. Figure 1B shows what is probably the most influential multistore model—the Working Memory model of Baddeley and Hitch (Baddeley, 2000; Baddeley & Hitch, 1974). I will present a very brief summary of the findings that have been taken as evidence for a separation between a long-term store (LTS) and a short-term store (STS). The primary data come from studies of STM patients. These patients typically have grossly impaired verbal STM capacity of perhaps 2–4 items, combined with rela- tively intact LTM (Basso, Spinnler, Vallar, & Zanobio, 1982; Saffran & Marin, 1975; Shallice & Vallar, 1990; Shallice & Warrington, 1970; Vallar & Baddeley, 1984; Vallar, Di Betta, & Silveri, 1997; Vallar & Papagno, 1995; Vallar, Papagno, & Bad- deley, 1991; Warrington, Logue, & Pratt, 1971; Warrington & Shallice, 1969). Where it has been examined, these patients gen- erally have few problems with visuospatial STM tasks. The oppo- site pattern has also been observed. Hanley, Young, and Pearson (1991) reported a patient with impaired visuospatial STM but normal verbal STM. One source of evidence that STM patients have intact LTM is that, in general, these patients have little difficulty in learning new associations between familiar stimuli. However, they do have problems in learning new words (Badde- ley, Papagno, & Vallar, 1988; Basso et al., 1982; Bormann, Sey- both, Umarova, & Weiller, 2015; Dittmann & Abel, 2010; Freed- man & Martin, 2001; Trojano & Grossi, 1995; Trojano, Stanzione, & Grossi, 1992). The standard interpretation of this finding is that the complete phonological representation of new words must be held in a short-term store in order to be encoded into LTM. Indeed,
one of the central functions of STM is assumed to be to hold representations that do not yet exist in LTM (Baddeley, Gather- cole, & Papagno, 1998). Importantly, the constituent parts of these representations (perhaps features, phonemes or syllables) must be stored in the correct order. Not surprisingly, these patients also have problems in learning the order of new digit sequences (Bor- mann et al.). The same logic applies; the sequence must be held in STM so that a representation of the sequence can be presented to LTM.
Conversely, there are patients with medial-temporal lobe dam- age who have impaired LTM but relatively preserved STM (Bad- deley & Warrington, 1970; Cave & Squire, 1992; Drachman & Arbit, 1966; Scoville & Milner, 1957; Wilson & Baddeley, 1988). Ranganath and Blumenfeld (2005) expressed concerns over whether the patient data really do provide clear evidence for distinct stores. They drew attention to the fact that LTM patients with medial temporal lobe damage have difficulties with some STM tasks, and suggest that this “questions whether theories of memory need to propose neurally distinct stores for short- and long-term retention” (p. 374). However, in a later review of the literature, Jeneson and Squire (2012) pointed out that the impair- ment of LTM patients in STM tasks is only observed with supras- pan stimuli that exceed the capacity of STM. Under these circum- stances even neurologically normal individuals will necessarily have to rely on a combination of STM and LTM, so it should be no surprise that LTM patients have problems. Furthermore, the finding that LTM patients are sometimes impaired in STM tasks is fully consistent with the two-store view; short-term recall can clearly benefit from a contribution from LTM, even if the two are functionally separate. For example, according to redintegration accounts (Gathercole, Pickering, Hall, & Peaker, 2001; Hulme et al., 1997; Lewandowsky & Farrell, 2000; Saint-Aubin & Poirier, 1999a; Schweickert, 1993; Schweickert, Chen, & Poirier, 1999), information in LTM can be used to reconstruct degraded traces in an STS at recall. Thus, even though LTM may play no role in the maintenance of information in STS, it can potentially improve performance in STM tasks by aiding retrieval.
The most powerful behavioral evidence for a form of distinct short-term storage comes from the early work of Baddeley and colleagues (Baddeley, 1966a, 1966b; Baddeley & Ecob, 1970), which led to the development of the concept of a phonological store. The phonological store is assumed to hold speech-based representations and to have duration of just a few seconds. Infor- mation within the store can be refreshed by an articulatory control process (rehearsal) so as to prevent decay, and that same process can be used to recode visual information into a phonological form (Baddeley, Lewis, & Vallar, 1984). Together these for the phono- logical loop component of the Working Memory model (Figure 1B).
The critical evidence for a phonological store with a limited duration is that while memory confusions at short retention inter- vals are primarily phonological in nature, confusions at longer retention intervals tend to be semantic. In immediate serial recall, phonological similarity impairs order recall and can even improve item recall (Fallon, Groves, & Tehan, 1999) but semantic similar- ity has no impact on order recall (Saint-Aubin & Poirier, 1999b; Saint-Aubin & Poirier, 2000). Furthermore, when the items to be remembered are presented visually as opposed to auditorily, the phonological confusions can be eliminated if participants are re-
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quired to perform articulatory suppression during presentation (Baddeley et al., 1984; Murray, 1968; Peterson & Johnson, 1971). Articulatory suppression is assumed to occupy the articulatory control process and prevent it from being able to recode the visual input into a phonological form.
These findings provided the motivation for separate phonolog- ical and visual short-term stores in Baddeley and Hitch’s (1974) Working Memory (WM) model. More recently Baddeley (2000) has expanded the working memory framework to include a com- ponent called the episodic buffer (Figure 1B). The episodic buffer is responsible for temporary storage beyond the capacity of the model’s short-term storage systems, and for binding representa- tions across different modalities. One line of evidence supporting the need to add yet another memory system comes from studies of prose recall. For example, the STM patient PV had an auditory word span of one but could remember up to five words when they formed a meaningful sentence (Vallar & Baddeley, 1984).
The strongest evidence for a separate STS does not require carefully controlled laboratory experiments at all. The mere fact that we can repeat nonsense words like ‘blontestaping’ that we have never heard before shows that memory cannot be based simply on activating preexisting representations in LTM. Although there may well be preexisting representations of phonemes, fea- tures or syllables, these are not sufficient to construct a mnemonic trace of a previously unencountered nonsense word.
Short-Term Memory and Working Memory
The terms STM and working memory (WM) are often used interchangeably, and also inconsistently. In this article the primary focus is on whether there are distinct short- and long-term stores. Working memory is usually thought of as a much broader concept, often encompassing processing as well as storage. For example, both the Baddeley and Hitch (1974) and the Cowan (1988) WM models include a central executive component which can operate on the contents of STM (see figure). In the Baddeley and Hitch model, modality-specific short-term stores form part of the overall WM system. The distinguishing feature of WM is that it provides a ‘mental workspace’ (Logie, 2003) that can hold information in a temporary form that can be manipulated and updated. Although there are different views on exactly what constitutes WM (for review see: Aben, Stapert, & Blokland, 2012), the common feature of these views is that rather than being simply a passive store, WM is a system that allows information to be actively manipulated. For example, in the context of visual Luck and Vogel (2013) defined WM “as the active maintenance of visual information to serve the needs of ongoing tasks” (p. 392). Baddeley (1992) described WM as a “system that provides temporary storage and manipulation of the information necessary for such complex cognitive tasks as language comprehension, learning, and reasoning.” (p. 556).
Although this distinction between passive stores and an active mental workspace is widely observed, some authors also use the broader term WM when describing studies that involve only pas- sive storage. This is particularly so in the case of work on visual STM. In contrast, Nee and Jonides (2013) use the term STM to refer to all memory over the short term, whether active or passive. This includes the ‘activated LTM’ component of Oberauer’s (2002, 2009) three-state model. One would more commonly ex- pect this broader conception to be referred to as WM. Ericsson and
Kintsch (1995) add further complexity by proposing that there is a form of long-term WM. Although these terminological inconsis- tencies can lead to confusion, our concern here is with the nature of the storage mechanisms themselves rather than the higher level cognitive processes that might operate of the contents of such stores. Nevertheless, it is worth pointing out that WM tasks like reasoning or language comprehension will necessarily recruit wide-ranging neural and cognitive processes that will simultane- ously engage both short- and long-term storage systems.
Interactions Between STM and LTM
Although multistore models have distinct short- and long-term stores, this does not imply that there are distinct short- and long- term tasks that tap exclusively into short- or only long-term mem- ory. Atkinson and Shiffrin (1968) wrote that “According to our general theory, both STS and LTS are active in both STS and LTS experiments” (p. 101). There is no particular point in time that would mark a transition between tasks that only involve an STS and those that involve only an LTS. Even under the view that there are separate short and long-term storage systems, the two systems should operate in concert. Interactions between LTM and STM have already been mentioned in the context of patients with deficits in STM or LTM. Long-term learning of novel words or digit sequences depends on STM, and performance in STM tasks is influenced by information in LTM. For example, although STM is predominantly phonological, performance in STM tasks is nev- ertheless influenced by lexical or semantic factors, or by other information stored in LTM. For example, words are recalled better than nonwords (Brener, 1940; Hulme, Maughan, & Brown, 1991), high-frequency words are recalled better than low-frequency words (Gregg, Freedman, & Smith, 1989; Hulme et al., 1997; Watkins & Watkins, 1977), concrete words are recalled better than abstract words (Bourassa & Besner, 1994; Walker & Hulme, 1999), sentences are recalled better than random word lists (Brener, 1940), sequences of letters are recalled better when they have a closer approximation to the statistics of English (Baddeley, 1964), and lists constructed from familiar sequences are recalled better than lists composed of unfamiliar sequences (Botvinick, 2005; Botvinick & Bylsma, 2005; Mathy & Feldman, 2012).
Some have interpreted this as evidence for a version of the activation view in which STM depends on activation in LTM language networks (Acheson, MacDonald, & Postle, 2011; Poirier, Saint-Aubin, Mair, Tehan, & Tolan, 2015). An alternative view is that although there is a separate STS, long-term semantic memory is activated in STM tasks, and the sustained semantic activation is fed back to STM to aid retention (Acheson, MacDonald, et al., 2011; Huttenlocher & Newcombe, 1976; Jefferies, Frankish, & Lambon Ralph, 2006a, 2006b; Jefferies, Frankish, & Noble, 2009; Patterson, Graham, & Hodges, 1994; Poirier et al., 2015; Savill, Metcalfe, Ellis, & Jefferies, 2015; Stuart & Hulme, 2000). This is sometimes referred to as semantic binding. Both of these possibil- ities run into exactly the same problems as the view that STM is activated LTM. Although almost all of the data comes from serial recall tasks, there is no indication of how simply activating se- mantic memory could code serial order.
The alternative view is that any benefit conferred by LTM occurs only at recall and operates by means of the kind of redin- tegration process described earlier (Schweickert, 1993). Redinte-
gration is most commonly thought of as operating at the level of individual items. For example, a degraded mnemonic trace might be more likely to be reconstructed as a high-frequency word than as a low frequency word. Consistent with this view, factors such as lexicality, word frequency, and semantic information affect recall of item information but not order information (e.g., Poirier & Saint-Aubin, 1996; Saint-Aubin & Poirier, 1999b). However, Acheson, MacDonald, et al. (2011) reported a semantic effect on order recall. They combined a serial recall task with a secondary task requiring participants to make either semantic or orientation judgments about pictures. The semantic tasks led to more order errors than the orientation task, and produced more errors for word list than for nonword lists. They concluded that the semantic task interfered with the temporary activation of semantic representa- tions within the language production architecture that could sup- port STM. According to this view, nonwords would be unaffected by the nature of the secondary task as they have no semantic representations. Acheson et al. acknowledge that it may well be possible to explain their results in terms of redintegration, but they suggest that redintegration should operate at the item level and not benefit memory for order. However, the Bayesian framework presented by Botvinick (2005) was specifically designed to explain how information in LTM could help recover order information. In this framework, any information available from LTM, whether general LTM or a specifically linguistic memory, could potentially influence retrieval of both item and order information. Therefore it is still possible that their results could be explained by redintegra- tion. From a psycholinguistic perspective, it would seem that listeners must necessarily form an integrated memory representa- tion that combines phonological, syntactic and semantic informa- tion, although establishing exactly how those representations are stored and interact with each other remains a challenge.
A further form of interaction between LTM and STM happens at encoding. In the Baddeley and Hitch working memory frame- work, visually presented words must be recoded into a phonolog- ical form in order to be stored in the phonological store, and this recoding process must involve contact with representations in LTM to generate the necessary phonology. As least in the case of verbal STM, maintenance of information is helped by rehearsal which involves recycling information in STS. At each phase in the recycling process there is an opportunity for LTM to be involved in the reconstruction of degraded traces in STS. Furthermore, if items that are being rehearsed are thought of as being in the focus of attention, they must inevitably make contact with the same LTM representations that would be involved in the perception of those items.
Finally, long-term learning is not restricted to situations where there is an explicit intention to learn. Implicit learning occurs even in tasks which ostensibly only require STM. Long-term learning, and hence, access to LTM, must take place continuously if we are to be able to learn about the relationships between events occurring too far apart to be held within STM. For example, in the classic Hebb (Hebb, 1961) learning paradigm, performance in serial recall of lists of verbal material improves over successive repetitions. The implication of this is that LTM must be continuously engaged even in what might appear to be ‘pure’ STM tasks, so that some long-term learning can take place on the very first encounter with a list. If it did not, then every occurrence of the list would
effectively be treated in exactly the same way as the first encounter and learning could never begin.
Taking these factors together, it is very difficult to imagine any set of circumstances in which LTM will not be involved to some degree in what might seem to be a pure STM task. As we will see below, the fact that LTM cannot simply be ‘turned off’ in STM experiments has implications for the interpretation of neuroimag- ing studies that have been presented as evidence against multistore models.
As STM and LTM have to perform similar functions, they are likely to share similar features. In particular, both involve basic processes such as encoding, retention, and recall. Both are subject loss of information through decay or interference, and both will be impaired when items to be remembered are similar. Brown, Neath, and Chater’s (2007) SIMPLE (scale invariant memory, perception and learning) model emphasizes these shared properties. Their model illustrates how a general principle of scale-independent similarity can be applied to simulate a range of key empirical findings in both STM and LTM without the need to make any distinction between STS and LTS. However, by focusing on the commonalities their model is unable to account for critical data such as the neuropsychological dissociations seen in STM patients or the change in the representational basis between STM and LTM. The success of the model is attributable to the fact that it embodies broad principles that apply to memory and perception quite gen- erally. If these principles are indeed general they would be ex- pected to apply equally well to separate short- and long-term stores. There is no contradiction between general principles and separate stores.
Cognitive models of STM as activated LTM. Atkinson and Shiffrin’s, 1971 paper is considered to be the classic statement of a two-store model. Figure 1A, based on the first figure in their paper, represents STS and LTS as separate boxes. Despite this they also say that “One might consider the short-term store simply as being temporary activation of some portion of the long-term store” (p. 83). More directly, Shiffrin (1975) wrote that “STS is the activated subset of LTS” (p. 214). Similarly, Norman (1968) talks about primary and secondary storage but also states that they “are different aspects of one large storage system” (p. 535). However, the theoretical force of these statements is unclear. Nothing seems to rest on this assumption and there is no discussion of its moti- vation or theoretical implications. This idea was developed further by Cowan (1988) who is regularly cited as supporting the idea that STM is activated LTM. Cowan stated quite clearly that “short-term storage should be viewed as an activated subset of long-term memory” (Cowan, 1988, p. 185), where short-term storage in- cludes both the phonological store, and the visuospatial sketch pad. Additionally, in his model, a subset of activated LTM corresponds to the focus of attention (Figure 1C). However, on closer reading, much of what Cowan says has close parallels with the Baddeley and Hitch multistore model.
In later writings, Cowan and Chen (2008) state that “We thus propose that although the mechanisms of short-term memory are separate from those of long-term memory, they are closely related” (p. 104). They also acknowledge that “A phonologically based storage and rehearsal mechanism, such as the phonological loop mechanism of Baddeley (1986), may come into play primarily when items have to be recalled in the correct serial order” (p. 94) and “The phonological storage mechanism may be another in-
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stance of the use of the focus of attention to assemble a new structure in long-term memory” (p. 95). Cowan and Chen also appreciate that some extra mechanism is required to store novel information, such as serial order, that may not already be repre- sented in LTM. In common with the WM model, Cowan’s model has a central executive which, among other things, is involved in “the maintenance of information in short-term memory through various types of rehearsal” (Cowan, 1988, p. 171). Cowan (2008) wrote that “Baddeley’s (2000) episodic buffer is possibly the same as the information saved in Cowan’s focus of attention, or at least is a closely similar concept.” At the very least then, Cowan’s model has the following components: LTM, an episodic buffer, a phonological store, and a rehearsal process controlled by a central executive. These would seem to correspond very closely to the components of Baddeley and Hitch’s (1974) multistore WM model. Given that not all short-term storage in Cowan’s model is supported solely by activated LTM, the crucial question then is
what is the remaining force of the claim that STM is activated LTM? Is there any part of the process of retaining information over the short-term that can be served simply by activating LTM? One factor that makes it hard to answer this question is the absence of a computational specification of what it means for LTM to be activated, and of how that activation then supports memory. As Cowan’s position has evolved to accommodate a broader range of behavioral data, it has had to respect the fact that very little of that data can be explained purely in terms of activation. His theoretical position no longer equates STM directly with activated LTM.
Oberauer (2002, 2009) has proposed a three-state model which also gives a central role to activated LTM (Figure 1D). He makes an additional distinction between activated LTM and a direct access region. A similar three-state model has been proposed by Nee and Jonides (2013). Oberauer views LTM as an associative network in which related items can automatically activate each other. A subset of those activated items corresponds to a region of
Figure 1. (A) Atkinson and Shiffrin’s (1971) model of STM. (B) Baddeley and Hitch’s working memory model (Baddeley, 2000). (C) Cowan’s (1988) model of memory and attention. (D) Oberauer’s (2002) model of working memory. Nodes and lines correspond to long-term memory representations. Black nodes are activated. Nodes within the large oval are in the direct access region. One node is in the focus of attention.
direct access, and items in the direct access region can be accessed immediately. Within the direct access region a smaller set of items is in the focus of attention. It is not clear whether the direct access region should be assumed to be a region of LTM. I will return to this question later.
Is there neuroimaging evidence for STM as activated LTM? Historically, much of the debate as to whether there are separate long- and short-term stores has focused on whether various ma- nipulations have different effects on long-term and short-term retention. For example, are there differences in the form of the serial position curve observed over different retention intervals? Wickelgren (1973) reviewed the behavioral data available in the early 1970s and argued that although the evidence favored the two-store account “the vast majority of all the cited evidence is worthless for making the distinction between short and long traces” (p. 426). Very little has changed since then. But might neuroimaging data be able to provide insights beyond those that can be had from behavioral data? If it could be shown that brain regions known to be responsible for LTM are activated during STM tasks, surely this would be evidence that those LTM regions were supporting STM? This unsound line of reasoning provides the rationale for the design and interpretation of a number of neuroimaging studies which have been presented as providing evidence that STM is simply activated LTM.
A flavor of the claims made in some neuroimaging papers can be found in the following quotations: “This result implies that activated long–term memory provides a representational basis for semantic verbal short-term memory, and hence supports theories that postulate that short- and long-term stor