Memory – one process or many

Memory, a fundamental cognitive process, can be defined as the acquisition and retention of information (Loring, 1999). It involves a range of capacities (Roediger, Marsh & Lee, 2002) and at a general level, there are several terms describing different forms or kinds of memory, and a distinction is often made between short-term and long-term memory.

Paller (2000) explains that memory research traditionally has been segregated into (a) research on the cognitive organisation of memory and (b) research on the brain basis of memory. Those theories of memory that are generally concerned with the way in which memory is organised can be broadly divided into systems theories, concerned with the architecture or structure of memory and process theories, concerned with the activities or processes involved (e.g., Eysenck & Keane, 2013). In more recent memory research, however, there is a trend towards using neural information to inform theories

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of memory, giving rise to neurocognitive models of memory which go some way towards reconciling the traditional cognitive and brain-based strands of memory research.

An early model of memory was the multistore model of memory, also known as the modal model (Atkinson & Shiffrin, 1968), a structural model in which memory is proposed to consist of three stores;

a sensory register, a short-term memory (STM), and long-term memory (LTM). Information was proposed to pass through these in a linear way. Thus, it is a type of information processing model. In this model, if maintenance of the memory through rehearsal does not occur, information will be lost from STM through a process of displacement or decay. Support for the model was provided by experimental psychology studies demonstrating primacy (wherein, relative to mid-list words, words at the beginning of a list are more easily recalled) and recency effects (wherein, compared to mid-list words, words near the end of a list have a higher probability of being recalled; Healy & McNamara, 1996). Support also comes from findings of oft-cited neuropsychological case-studies in the literature such as patient HM (Milner & Corkin, 1968) and patient KF (Shallice & Warrington, 1975), both of whom showed dissociation between STM and LTM. Anterograde amnesia was observed in patient HM following resection of HM’s medial temporal lobe structures for the relief of medically intractable epilepsy, affecting his declarative and episodic memory but leaving his short-term memory intact. Prior to this, memory functions were believed to be distributed in the cortex (Eichenbaum, 2013).

Performance of patient KF in a series of experiments showed that KF had a greatly reduced short term memory capacity which could not be attributed to a retrieval failure, however his performance on long-term memory tasks was normal.

Evidence has since emerged, however, that STM and LTM do not operate in a single uniform fashion (Davelaar, Goshen-Gottstein, Ashkenzai, Kaarmann, & Usher, 2005). Furthermore, STM comprises different components such as a central executive component and visuospatial component (Baddeley &

Hitch, 1974) and LTM also consists of different types of memory (e.g. episodic: memory of events;

procedural: knowledge of how to do things and semantic: general knowledge). It has also been shown that simple rehearsal is too simplistic an account for the transfer of memory from STM to LTM and that the modal model ignores other factors and processes of memory such as motivation and elaboration.

These limitations were subsequently addressed by more sophisticated models of memory that better took account of the interaction of various processes involved in memory. Two main or influential models in this regard are the Levels of Processing (LOP) Model (Craik & Lockhart, 1972) and Baddeley’s Working Memory (WM) model (Baddeley & Hitch, 1974).

The LOP model of memory is based on the theory that the way that information is encoded affects how well it is remembered. It proposes that processing of memories can take place at a shallow level

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(maintenance rehearsal leading to short-term retention) or a deep level (involving semantic processing and elaboration rehearsal, e.g. images and associations), leading to better retention and recall.

Although the concepts of depth of procession and elaboration have been criticised as ill-defined (Nelson, 1977; Baddeley, 1978) and difficult to demonstrate empirically due to circular reasoning (the tendency to define depth in terms of the memory outcome) (Proust, 1993), the LOP model improves on the modal model of memory by accounting more comprehensively for processes involved in the transfer of memory from STM to LTM and it paved the way for the development of an influential model of working memory (Baddeley & Hitch, 1974).

Working memory is a system that temporarily stores and maintains information in the form of internal representations and manipulates these representations (Nilsson, 2003). According to Schacter and Tulving (1994), it is one of five major memory systems; the other four being semantic memory, episodic memory, procedural memory, and the perceptual representation system.

Connectionist models, also known as Parallel Distributed Processing (PDP) models, are a class of computational models often used to explain memory storage and retrieval, using an information processing approach (McClelland & Rummelhart, 1988). As a class of model, it represents a paradigm shift from previously outlined models of memory that describe a serial and linear account of how memory works. In this model, cognitive processes are described as networks in which the elements have multiple links. According to these models, ‘memory’ is the activation of these connections in different areas (the “distribution”) at the same time (“parallel”). The patterns of the activations that occur at and between a multitude of nodes in the brain give rise to cognitive representations such as memory and knowledge. The strength of such memory traces and knowledge is aided by the strength of the connections activated between the relevant parts of the brain.

More recent neurocognitive models of memory build upon these earlier cognitive models and attempt to incorporate knowledge of the neural basis of memory into the framework for understanding the organisation of memory. A brief overview of some of these models is presented below.

The classical consolidation model proposed by Larry Squire and colleagues (Squire, 1987; Zola-Morgan

& Squire, 1990; Squire & Alvarez, 1995; Squire & Zola, 1996; Squire, 1992) is one such influential neurocognitive model. The term “consolidation” was coined around the turn of the century by Muller

& Pilzecker (1900) to describe a time-dependent process needed to assimilate an experience and store it permanently as a memory that would not be easily disrupted. According to the model, consolidation is distinguished into two specific processes; synaptic consolidation, which is synonymous with late-phase long-term potentiation and occurs within the first few hours after learning and systems consolidation, where hippocampus-dependent memories are purported to become independent of the

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hippocampus over a period of weeks to years and are moved to the neocortex in a more permanent form of storage (Roediger, Dudai & Fitzpatrick, 2007). A third process, reconsolidation, refers to previously-consolidated memories becoming labile again through reactivation of the memory trace (Nader, Scafe & Le Douz, 2000; Sara, 2000). Support for the memory consolidation model is forthcoming from a variety of sources, including lesion studies of human patients (e.g. Squire, Haist &

Shimamura, 1989; Kapur, 1999), experimental animal studies (Anagnostaras, Maren & Fanselow, 1999) and computational-based neural modelling (McClelland, McNaughton & O’Reilly, 1995).

The standard consolidation model was substantially informed by lesion studies of individuals with damage to their medial temporal lobe or diencephalic nuclei, most notably following Scoville and Milner’s 1957 publication on the effects of excision of the anterior and medial temporal lobes bilaterally to control intractable epilepsy in patient HM. These individuals displayed normal short-term memory.

Similarly, it was observed that older (remote) memories, both autobiographical and semantic, were stored and could be retrieved readily without the medial temporal lobe (Corkin, 1984). These observations were interpreted as showing that the function of the medial temporal lobes and related diencephalic structures was not to process short-term memories or to store long-term memories but, rather, was to help consolidate memories in other brain regions and to encode, store and retrieve them until consolidation was complete (Squire, 1992). The standard consolidation model, therefore, argues that the hippocampus is a time-limited memory structure for all forms of memory.

This standard account characterises “recent memories” as those that depend on both cortical and hippocampal networks. It draws distinctions between declarative and non-declarative (procedural) memory systems. Declarative memory pertains to the conscious recollection of complex facts and personally-experienced events. Non-declarative or procedural memory, on the other hand, refers to non-conscious recollection of a diverse set of phenomena including skill learning, habit learning, simple forms of conditioning, various types of priming that can be measured in implicit memory tests and non-associative forms of learning like habituation and sensitisation (e.g. Squire & Zola, 1996). This distinction based on research on amnesic patients that showed retained ability to be trained on tasks and to exhibit learning without the patient having been aware that the training had ever taken place (Squire, 1986). As noted below, a declarative memory does not reside in a single location, but rather depends on a dynamic network of neurons. The standard consolidation model proposes that procedural knowledge is consolidated in some cases by the extrapyramidal motor system (Squire, 1986).

According to the standard account, when new information is encoded and registered, memory of these new stimuli are retained in both the hippocampus and neocortical regions for allegedly up to one week,

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representing the hippocampus-dependent stage (Frankland & Bontempi, 2005). During this time, a process whereby declarative memories outgrow their dependence on cortico-hippocampal networks to become cortically self-reliant occurs. This process is believed to involve the hippocampus “teaching”

the cortex more and more about the information. Recall of the information further strengthens the connection between the hippocampus and surrounding cortex, thus enabling the memory to become hippocampal-independent. Since it may involve increased connectivity among the components of the memory in the cortex, the process is sometimes referred to as cross-cortical consolidation (e.g. Paller, 2002; 2009). Medial temporal-lobe structures are also believed to play a role in the consolidation of memories within the neocortex by providing a binding area for multiple cortical regions involved in the initial encoding of the memory (Squire & Alvarez, 1995). This “training” of the neocortex by the hippocampus allows new information to be assimilated into neocortical networks with a minimum of interference. A recent revision of this account from a neurocomputational perspective (McClelland, 2013), a factor believed to influence the rate of consolidation more than a fast or slow rate of learning, is the amount of prior knowledge that is available about the material to be learned (Tse et al., 2007;

van Kesteren, Ruiter, Fernandez & Henson, 2012). In other words, if the information to be learned is consistent with prior knowledge, neocortical learning can become more rapid.

The standard model also proposes the formation of new cortical representations that function to represent the gist or higher-order meaning of the memory while simultaneously enhancing the coherence of the set of neocortical storage sites. How exactly this occurs is somewhat in debate, although Wiltgen et al. (2010) favour the view that consolidation entails an active process of extracting the gist or pattern from what was learned, although forgetting individual instances (including the most recent instance). However, Squire, Genzel, Wixted, and Morris (2015) recognise that it is unclear whether a qualitative process/mechanism of gist extraction is in practice, required, and that the possibility that there are qualitative changes in the character of memory during consolidation is currently an active area of research.

This standard model acknowledges that memory is reconstructive and vulnerable to errors, or false remembering (Schacter & Dodson, 2001). As previously mentioned, it also recognises that under some conditions, long-term memory can transiently return to a labile state (and then gradually stabilise), a process known as reconsolidation (Nader et al., 2000; Sara, 2000).

The consolidation process for relatively new memories is interrupted by retrograde amnesia so that enough consolidation to produce a stabilised cortical memory is not achieved. It follows that these memories cannot, therefore, be accessed in the absence of retrieval mechanisms that depend on the

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hippocampus and related structures. However, if enough consolidation has otherwise been achieved, an old or long-term memory can be retrieved via cortical mechanisms.

The standard model makes no distinction with respect to consolidation among different types of explicit memory, be they spatial or non-spatial, episodic or semantic, recollective or familiar (Squire &

Zola, 1998; Squire, 2004). All are dependent on the hippocampal complex/medial temporal lobe (HC/MTL) for the duration of the consolidation period, after which time they can be retained and retrieved independently of it. Thus, damage to the HC/MTL and diencephalon leads to a graded, temporally limited, retrograde amnesia for both episodic and semantic memory, whether autobiographical or spatial. Memories acquired most recently are most severely affected, with remote memories, having already been fully consolidated before the brain insult or onset of amnesia, being retained normally (Squire, 1992; Squire & Alvarez, 1995).

The standard account of consolidation has also been investigated in healthy volunteers using neuroimaging methods like PET or fMRI. Squire and colleagues (2015) explain that neuroimaging studies can establish whether a particular structure (e.g. the hippocampus, medial prefrontal cortex, or a network of structures) is active when recent and remote memories are retrieved, but this method does not conclude whether a structure is necessary for retrieval. Specifically, a temporal gradient of hippocampal activation (e.g. greater activation for recent than remote memories) might reflect a decreasing dependence on the hippocampus as memories age, but this might also reflect differences in the extent to which memories of different ages are relearned or re-encoded as they are recollected.

Imaging studies used to explore how and under what conditions consolidation occurs, led to the proposed phenomenon of “neural replay.” This refers to the spontaneous recurrence of hippocampal activity that occurred originally during learning, a phenomenon supported by animal and human studies (e.g. Takehara-Nishiuchi & McNaughton, 2008; Peigneux et al., 2004).

To this end, Squire and colleagues (2015) cite the results of neuroimaging studies (Takashima et al., 2006; 2009; Yamashita et al., 2009; Furman et al., 2012; Harand et al., 2012) employing a prospective design that affords experimental control over the memories from different time periods. In such designs, participants learn similar materials at multiple different time points before scanning. The results of these prospective studies are also mixed in their support of the standard account of consolidation. For example, in the study by Takashima et al., (2006), participants memorised two sets of face-location associations; one was studied 24 hours before testing (remote memories) and others studied 15 minutes before testing (recent memories). Activity in the hippocampus decreased (and activity in the neocortex increased) as a function of time after learning. At the same time, functional connectivity between the hippocampus and cortical areas decreased over time, whereas connectivity

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within the cortical areas increased. This temporal gradient is shorter than what is typically observed in lesion studies, but Squire and colleagues state that these findings are nevertheless in agreement with the idea that the hippocampus becomes less important for memory with the passage of time.

In another prospective study, by Furman et al. (2012), participants were tested on their memory of documentary clips. When memory was tested by recognition, a sign of memory consolidation, activity in the hippocampus was observed to decline as time passed over a period of months. By contrast, hippocampal activity remained stable across time when memory was tested by recall. Cortical activity also decreased as time passed. The findings of this study suggest a continuing role for the hippocampus in long-term memory, in contrast to the fundamental tennet of the standard model of consolidation.

There remains, however, a concern regarding the use of prospective designs for the investigation of memory that, by the time memory is tested in the scanner, many older memories will have been forgotten. Thus, the possibility exists that surviving remote memories may be relatively durable and are being compared with a mixture of durable and less durable recent memories. One study (Yamashita et al., 2009) addressed this potential issue, by monitoring activity in the hippocampus and temporal neocortex as participants recalled two sets of paired-associate figures that they had memorised at two different times – 8 weeks before testing (remote memories) and just before testing (recent memories).

Imaging results showed that an area in the right hippocampus was more active during retrieval of new memories than old memories, whereas in the left temporal neocortex, the opposite pattern occurred.

These results were considered consistent with the standard account of memory consolidation, i.e. a decreasing role of the hippocampus and an increasing role of the neocortex as memories age across a period of 50 days. Recent evidence, however, has not always been consistent with the standard model of consolidation. Neuroanatomical and functional considerations are at the core of the discrepancy concerning consolidation and the representation of remote memories in the brain (Moscovitch et al., 2005).

The main issue in relation to the standard consolidation model is the fact that retrograde amnesia for episodic (including spatial) memory is prolonged yet memory is relatively preserved for semantic (including spatial) memory (Nadel & Moscovitch, 1997, 1998; Moscovitch & Nadel, 1998; Fujii, Moscovitch & Nadel, 2000). Indeed, Kinsbourne and Wood (1975) argued that retrograde amnesia is a deficit only of episodic (autobiographical) memory that affects recent and remote memory equally.

Retrograde amnesia for autobiographical episodic memory can extend for decades, or even a lifetime – longer than biologically plausible for a consolidation process to last. In contrast, retrograde amnesia for semantic memory is less extensive and is often temporally graded (Fujii et al., 2000). Thus,

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contrasting to the argument of the standard consolidation model, non-spatial semantic and episodic memories are affected differentially by lesions producing retrograde amnesia (Warrington, 1996).

Semantic memories themselves, depending on their characteristics, may also be differentially affected by lesions. Evidence reviewed by Moscovitch and colleagues (2005) suggests that it is useful to distinguish between those spatial memories that consist of detailed perceptual-spatial representations of experienced environments (corresponding to episodic autobiographical memory) and those that consist of schematic representations of the topography of the environment (corresponding to semantic memory). The authors conclude that schematic (semantic) spatial memories can survive damage to the HC)/MTL), but perceptually detailed (episodic) spatial memories cannot.

To account for the evidence at odds with the standard model, Nadel and Moscovitch (1997) proposed a multiple trace theory (MTT) of memory. According to the MTT and in line with standard consolidation model, the HC and possibly the diencephalon rapidly encodes all information that is consciously apprehended (Moscovitch & Umilta, 1990; Moscovitch, 1992) and binds the neocortical (and other neurons) that represent that experience into a memory trace. In line with reasoning in the standard consolidation model, formation and consolidation of these memory traces is relatively rapid, lasting for the order of seconds or, at most, days. However, in the MTT model, in contrast to the standard consolidation model, there is no prolonged consolidation process that is proposed to slowly strengthen the neocortical component of the memory trace, so that with time, the trace becomes independent of the HC/MTL. Instead, MTL has a static role; each time an old memory is retrieved, a new hippocampally-mediated synaptic connection between the MTL and neocortex is created. Since older memories are represented by stronger, or a greater number of, HC/MTL neocortical traces than are new memories, they are less susceptible to disruption from restricted lesions of the MTL. This produces the temporally graded memory loss that is observed.

Whereas each autobiographical memory trace is unique, the creation of multiple, related traces facilitates the extraction of the neocortically-mediated information common to them and that is shared with other episodes. This information is then integrated with pre-existing knowledge to form semantic memories that can exist independently of the HC/MTL. Thus, knowledge about the world, about people

Whereas each autobiographical memory trace is unique, the creation of multiple, related traces facilitates the extraction of the neocortically-mediated information common to them and that is shared with other episodes. This information is then integrated with pre-existing knowledge to form semantic memories that can exist independently of the HC/MTL. Thus, knowledge about the world, about people