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Conscious and Unconscious Memory

 

 

 

John F. Kihlstrom

University of California, Berkeley

Jennifer Dorfman

University of California, Berkeley

Lillian Park

State University of New York

College at Old Westbury

 

 


 

 

Note: This is a longer, more fully referenced version of an article which wil appear in S. Schneider & M. Velmans (Eds.) Blackwell Companion to ConsciousnessOxford, U.K.,, 2e. : Blackwell

 

 


Abstract

Conscious recollection appears to be governed by seven principles: elaboration, organization, time-dependency, cue-dependency, encoding specificity, schematic processing, and reconstruction.  However, these same principles may not apply to unconscious, or implicit, memory.  Implicit memory is most commonly reflected in priming effects which occur in the absence of conscious recollection.  Dissociations between explicit and implicit memory have been observed in patients suffering various sorts of brain damage, in other forms of amnesia, in behavioral performance of neurologically intact subjects, and in brain-imaging studies of memory.  The most popular interpretation of these dissociations holds that explicit and implicit memory are mediated by separate and independent brain systems.  However, there are also compelling interpretations in terms of dual processes operating on the contents of a single memory system. 

 

Keywords: amnesia; declarative knowledge; explicit memory; implicit memory; priming; procedural knowledge; source amnesia


Conscious and Unconscious Memory

            In the earliest years of scientific psychology, research focused on immediate conscious experience, in the form of sensations and percepts analyzed first by psychophysicists like Weber and Fechner, physiological psychologists like Helmholtz, and structuralists like Wundt and Titchener.  Wundt believed that “higher” mental processes, such as memory, were not amenable to experimental study.  But Hermann von Ebbinghaus proved him wrong in 1885: by counting repetitions and calculating savings in relearning, Ebbinghaus invented the verbal-learning paradigm that has dominated the scientific study of memory ever since (Anderson, 1985; Gorfein & Hoffman, 1987; Tulving & Craik, 2000).

 

Knowledge and Memory

We speak of “memory” but in fact there appear to be many memories.  The “modal” multistore model of memory (Atkinson & Shiffrin, 1968; Waugh & Norman, 1965) postulates a number of distinct storage structures (or systems) in the mind.  These include modality-specific sensory registers (e.g., iconic and echoic memory); primary, short-term, or working memory; and secondary or long-term memory.  The distinction between short- and long-term memory is more a matter of distraction than retention interval.  Short-term memory applies while our attention is focused on something; long-term memory applies after our attention has turned elsewhere.  The term “working” memory emphasizes the fact that short-term memory is not merely a passive repository of stimulus information; it is where memories are actively used in ongoing cognitive processing (A. Baddeley, 1992, 2012; A. D. Baddeley & Hitch, 1974).


For most people, “memory” means long-term memory.  As James put it in the Principles, “Memory proper... is the knowledge of a former state of mind after it has already once dropped from consciousness; or rather it is the knowledge of an event, or fact, of which meantime we have not been thinking, with the additional consciousness that we have thought or experienced it before.”  At the same time, short-term or working memory is often identified with consciousness.  Primary memory is sometimes viewed as a separate memory system from secondary memory; in other theories, primary memory is identified with those representations stored in long-term memory which are currently in a state of activation. 


The knowledge stored in long-term memory comes in two broad forms (Anderson, 1976).  Declarative knowledge constitutes our fund of factual knowledge, and can be represented by sentence-like propositions.  Procedural knowledge consists of our cognitive repertoire of rules and skills, and can be represented by “if-then” structures known as productions.  Within the domain of declarative knowledge, we can distinguish episodic memory, or autobiographical memory for events that have occurred in our personal past, and semantic memory, a sort of impersonal mental dictionary.  Procedural knowledge can be further classified into motoric and perceptual-cognitive skills.  The declarative-procedural distinction has its immediate origins in computer science and artificial intelligence (Winograd, 1975), but can be traced back to Ryle’s (Ryle, 1949) distinction between “knowing that” and “knowing how”, and Bergson’s (Bergson, 1911) assertion that “the past survives in two forms” -- as recollections and as habits.  Again, episodic memory is what most people mean by “memory”, as opposed to “knowledge”.  Conceptually, an episodic memory trace contains a description of some event, the unique spatiotemporal context in which that event occurred, and reference to the self as the agent or patient, stimulus or experiencer, of that event (Kihlstrom, 1995, 1997a).


A popular framework for memory research is stage analysis, according to which memories are analogous to books in a library, or the information contained within them (Crowder, 1976; Melton, 1963).  Mental representations of events are encoded as memory traces, which are retained in memory storage; these traces are then subject to retrieval.  Stage analysis gives rise to the distinction is between availability and accessibility (Tulving & Pearlstone, 1966): Encoded memories, available in memory storage, may not be accessible when retrieval is attempted.  On the other hand, they may operate unconsciously, even when conscious remembering fails.  Hence the distinction between explicit memory, or conscious recollection, and implicit memory, or the influence of a past event on the person’s experience, thought, or action, in the absence of, or independent of, conscious recollection of that event (Schacter, 1987).

 

Seven (Plus or Minus Two) Principles of Conscious Recollection

            For most of the century following Ebbinghaus, the psychology of memory was concerned with conscious recollection – with our ability to recall or recognize events that had occurred in the past.  From this research emerged a small set of principles that largely govern how human memory operates:


1.    Elaboration: Memory is a function of the degree to which an event is related to pre-existing knowledge at the time of encoding (F.I.M. Craik & Lockhart, 1972). 

2.    Organization: Memory is also a function of the degree to which individual events are related to each other (Bower, 1970; G. Mandler, 1979).

3.    Time-Dependency: Memory generally fades with time, due to decay, displacement, consolidation failure, or interference among competing memory traces (Ballard, 1913).  On the other hand, memory consolidation itself takes time (Lecner, Squire, & Byrne, 1999; J. L. McGaugh, 1966; J.L. McGaugh, 2000).

4.    Cue-Dependency: Successful remembering is a function of the informational value of the cues provided at the time of retrieval (Tulving, 1974).

5.    Encoding Specificity: Remembering also depends on a match between the cues present at the time of retrieval match those processed at the time of encoding (Tulving & Thomson, 1973). 

6.    Schematic Processing: Events that are relevant to currently active beliefs, expectations, and attitudes are remembered better than those that are irrelevant; among schema-relevant events, those which are incongruent with these mental schemata are remembered better than those which are congruent (Hastie, 1981).

7.    Reconstruction:  Memory reflects a mix of information contained in the memory trace and knowledge derived from other sources (Bartlett, 1932).  In the final analysis, memories are beliefs, and remembering an event is more like writing a story from fragmentary notes than reading it from a book.

 

Different classes of memory may operate according to somewhat different principles.  Although elaborative rehearsal seems to be necessary for encoding in long-term memory, for example, rote maintenance rehearsal will suffice to keep material active in short-term memory (F. I. M. Craik & Watkins, 1973).  Elaboration is critical for explicit memory, but less important for implicit memory (L.L. Jacoby & Dallas, 1981).  Forgetting from the sensory registers and short-term memory is produced by decay and displacement, which affect availability; forgetting in long-term memory appears to be a problem of proactive and retroactive interference, which affect accessibility (Anderson, 1974; Anderson & Reder, 1999).

 

Dissociating Explicit and Implicit Memory

            For most of its history, the scientific study of episodic memory was concerned mostly with conscious recollection, to the extent that it was concerned with consciousness at all, and the notion of unconscious memory was relegated mostly to the Freudian fantasyland.  But beginning in the 1960s, research began to suggest that the notion of unconscious memories was valid after all – if not in the Freudian form.  Of particular interest were studies of patients with the amnesic syndrome caused by damage to the hippocampus and related structures in the medial temporal lobe, or to the mammillary bodies and related structures in the diencephalon.  In a pioneering study, Warrington and Weiskrantz asked amnesic patients to study a list of familiar words (Warrington & Weiskrantz, 1968).  Compared to control subjects, the patients performed very poorly on standard tests of recall and recognition.  However, when they were presented with three-letter stems or fragments, and asked simply to complete the cues with the first word that came to mind, amnesics and controls were equally likely to complete the cues with items from the studied list.   


This is a priming effect, in which the processing of one item (e.g., at the time of study) influences the processing of another item (e.g., at the time of test).  In positive priming, the prime facilitates processing of the target; in negative priming, the prime inhibits processing of the target.  In this instance, the priming effect indicates that the studied items were encoded in memory, retained in storage, and influenced performance on the completion test.  The fact that equivalent levels of priming occurred in neurologically intact subjects, who remembered the priming episode normally, and amnesic patients, who had very poor memory, indicates that priming can be dissociated from conscious recollection. 


A later experiment by Graf et al. established a standard method for exploring dissociations between explicit and implicit memory (Graf, Squire, & Mandler, 1984). Tests of recall and recognition differ from the “guessing game” employed by Warrington and Weiskrantz on a number of dimensions, of which the most important is the informational value of the cues presented to the subjects.  For their explicit task, Graf et al. asked subjects to complete word-stems with items from the study lists; for the implicit task, subjects were asked to complete the stems with the first words that came to mind.  Amnesic subjects performed poorly on stem-cued recall, but normally on stem-completion, conforming the dissociation between explicit and implicit memory.  


On the basis of evidence like this, Schacter distinguished between two expressions of episodic memory: explicit and implicit (Schacter, 1987; see also Roediger, 1990).  Explicit memory refers to conscious recollection of a past event, as exemplified by performance on recall and recognition tests.  By contrast, implicit memory refers to any effect of an event on subsequent experience, thought, or action.  Priming is, of course, just such an effect.  The dissociation between priming and recall in amnesic patients indicates implicit memory can persist in the absence of explicit memory.  Subsequent research identified a number of different dissociations between explicit and implicit memory (for a more comprehensive review, see Reder, Park, & Kieffaber, 2009, who also note important exceptions to these outcomes). 


Probably the most obvious and convincing of these involve the amnesic syndrome and other forms of memory disorder.  By definition, these syndromes are marked by an impairment of explicit memory; but they also generally spare priming and other manifestations of implicit memory.  These conditions include anterograde amnesia associated with bilateral damage to the hippocampus and other structures in the medial temporal lobe (e.g., Schacter, 1987; Squire, 1992); anterograde  (Squire, Shimamura, & Graf, 1985) and retrograde (Dorfman, Kihlstrom, Cork, & Misiaszek, 1995) amnesia occurring as a consequence of electroconvulsive therapy (ECT) for depression; general anesthesia administered to surgical patients (Kihlstrom, Schacter, Cork, & Hurt, 1990 see Chapter 51); conscious sedation in outpatient surgery (Cork, Heaton, & Kihlstrom, 1996; see also Chapter 51); dementia, including Alzheimer’s disease (Salmon, Shimamura, Butters, & Smith, 1988); posthypnotic amnesia (Kihlstrom, 1980, 2007); and the “functional” or “psychogenic” amnesias encountered in genuine cases of dissociative disorder (Aarts & Custers, 2014; Kihlstrom & Schacter, 2000), including dissociative amnesia, dissociative fugue, and the interpersonality amnesia of dissociative identity disorder (also known as multiple personality disorder).  Normal age-related declines in memory primarily affect explicit memory, leaving implicit memory intact (Light & La Voie, 1993; Light & Singh, 1987).  And neurologically intact subjects show significant savings in relearning for items that, because of the long retention interval involved, they can neither recall nor recognize (Nelson, 1978). 


One of the most interesting of these dissociations is observed in source amnesia, where patients and subjects acquire new declarative and procedural knowledge, but have no conscious recollection of the learning episode (Brown & Murphy, 1989; Evans & Thorne, 1966; Schacter, Harbluk, & McClachlan, 1984; Shimamura & Squire, 1987). 


In the cases noted above, implicit memory can occur in the absence of explicit memory.  Conceptually similar “functional” dissociations can even be observed in individuals with normal memory, where implicit memory is in some sense independent of explicit memory (for a review, see Reder et al., 2009; Roediger & McDermott, 1993).  For example, a number of experimental manipulations have substantial effects on explicit memory, but little or no effect on implicit memory.  These include depth of processing at the time of encoding (Jacoby & Dallas, 1981); the generation effect (Jacoby, 1983); repetitions (Parkin, Reid, & Russo, 1990) and exposure duration (Jacoby & Dallas, 1981).  Implicit memory is less vulnerable to variations in retention interval (Jacoby & Dallas, 1981), and to interference effects (Graf & Schacter, 1987).  Still other manipulations affect implicit memory, but not explicit memory.  These include: a modality shift between study and test (Graf, Shimamura, & Squire, 1985); changing the font of a visual stimulus (Roediger & Blaxton, 1987); and changing the voice of an auditory stimulus (Church & Schacter, 1994).


Finally, neuroimaging studies indicate that performance of explicit and implicit memory tasks is associated with different patterns of brain activity (Schacter & Buckner, 1998).  For example, Schott et al. found that visual word priming was associated with decreased activity in the fusiform area, frontal, and extrastriate cortex; cued recall was associated with increased activity in posterior cingulate cortex, precuneus, and inferior parietal lobe (Schott et al., 2005; Schott, Richardson-Klavehn, Heinze, & Duzel, 2002).  A meta-analysis of fMRI studies showed clear evidence of medial-temporal/hippocampal activation during episodic encoding and retrieval (Spaniol et al., 2009).  Of course, the dissociation observed in amnesic patients also suggests that performance on explicit memory tasks relies on an intact hippocampus, and other structures in the medial temporal lobes, while priming is dependent on the cerebral cortex – a point to which we will return later.  


There are exceptions to these findings, which complicate the picture somewhat (Reder et al., 2009).  Consider, for example, the functional dissociation involving depth of processing, which is so well accepted that it has almost become part of the operational definition of implicit memory (you know that priming is an expression of implicit memory, as opposed to something else, if it is independent of depth of processing).  Two comprehensive meta-analyses of this literature, aggregating the studies, found that there was, indeed, an effect of depth of processing on priming, even if individual studies lacked the power to detect it (Brown & Mitchell, 1994; Challis & Brodbeck, 1992).  The effect was smaller on implicit than on explicit memory, but it was there nonetheless.  So, in this respect at least, implicit memory may not operate on different principles than explicit memory.


            Dissociations between explicit and implicit memory come in several forms (Dunn & Kirsner, 1988; Richardson-Klavehn, Gardiner, & Java, 1996; Teuber, 1955).  Most often, they take the form of single dissociations, in which a single independent variable – amnesia, experimental manipulation, or brain region -- affects one expression of memory, explicit or implicit, but not the other.  Statistically, however, single dissociations take the form of statistical interactions (i.e., between some independent variable and dependent variables measuring explicit and implicit memory), which are often difficult to interpret.  Long ago, for example, Chapman and Chapman pointed out that spurious interactions can emerge as artifacts of differential item difficulty (Chapman & Chapman, 1973, 1978).  Similarly, Loftus noted that non-crossover interactions (which is what single dissociations are) may be “removable” if the dependent variables are placed on the same scale of measurement (Loftus, 1978; Wagenmakers, Krypotos, Criss, & Iverson, 2012).  More practically, Graf et al. pointed out that differences between explicit and implicit memory are only meaningful if the cues presented at the time of test are matched for their informational value (Graf, Squire, & Mandler, 1984).  Comparing explicit free recall to implicit word-stem completion, for example, confounds the explicit-implicit dimension with cue information: word-stems have more informational value than free-recall tests.  A more appropriate comparison would pit stem-completion against stem-cued recall. 


For these and other reasons, double dissociations are the “Holy Grail” of cognitive neuropsychology and cognitive neuroscience.  Double dissociations take the form of a crossover interaction, in which a single independent variable has opposite effects on two dependent variables, and they allow firm conclusions that performance of the two tasks is mediated by distinct processes, cognitive modules, or brain systems.  Unfortunately, double dissociations are also exceedingly rare.  However, many ostensible double dissociations are not genuine crossover dissociations.  Rather, they are more like twin dissociations, in which one independent variable affects explicit but not implicit memory, while another affects implicit but not explicit memory.  As such, they are vulnerable to removability and the other problems discussed earlier. 

 

Taxonomic Issues

            Implicit memory is usually tested with a priming task, but priming comes in a number of different forms (Cofer, 1967; Roediger, 1990).  Most research on implicit memory has focused on repetition priming, in which the target of the priming test is a recapitulation or token, in whole or in part, of the prime itself.  For example, subjects might study a word like doctor and then be asked to complete the stem doc- or the fragment d-c-o- with the first word that comes to mind, to identify the word doctor when presented against a noisy background (perceptual identification), or to decide whether the letter string doctor is a legal word (lexical decision).  But semantic priming effects, also known as indirect priming, can also be observed when subjects who have studied a word like doctor are asked to give free associations to cues like nurse, or to generate instances of categories like occupations (McNamara, 2005).  Repetition priming can be mediated by a perception-based representation that is limited to the physical attributes of the prime and its configuration in space and time, but semantic priming requires a meaning-based representation that includes information about the semantic and conceptual features of the prime.  Semantic priming can be studied with the same tasks normally used to measure repetition priming, such as perceptual identification and lexical decision, provided that the target and prime are linked by meaning rather than physical similarity.  But it is more commonly studied with tasks such as free-association and category generation.


            Explicit and implicit memory are sometimes referred to as “declarative” and “procedural” memory (Cohen & Squire, 1980), or “declarative” and “nondeclarative” memory (Squire, Knowlton, & Musen, 1993), respectively.  The declarative-procedural usage was initially based on the view that preserved learning in amnesia was limited to procedural knowledge such as cognitive and motor skills, and an interpretation of priming and conditioning (some forms of which are also preserved in amnesia) as procedural in nature.  While some implicit expressions of memory may be mediated by procedural or nondeclarative knowledge, the declarative-nondeclarative distinction risks confusing the interpretation of explicit memories as representations that can be consciously “declared” with the propositional format in which declarative knowledge is represented.  Amnesic patients can acquire new declarative knowledge as well, provided that they do not have to remember the circumstances in which they learned it (as in source amnesia).  Furthermore, amnesia can also spare semantic priming, which is mediated by semantic memory -- which in turn is an aspect of declarative knowledge (Arndt, Passannante, & Hirshman, 2004; Barnier, Bryant, & Briscoe, 2001; David, Brown, Pojoga, & David, 2000; Gardner, Boller, Moreines, & Butters, 1973; Keane et al., 1997; Kihlstrom, 1980; Levy, Stark, & Squire, 2004).  Unfortunately, dissociations involving semantic priming have been much less studied -- with consequences for theories of implicit memory, as noted below. 


            Tests of explicit and implicit memory are sometimes referred to as “direct” and “indirect”, or “intentional” and “incidental”, respectively (Johnson & Hasher, 1987; Richardson-Klavehn & Bjork, 1988).  That is to say, recall and recognition test memory directly, while savings or priming tests memory indirectly.  This can cause confusion, as Cofer distinguished between “direct” (repetition) and “indirect” (semantic) forms of priming, raising the risk that repetition priming could be labeled as “direct-indirect” memory, and semantic priming as “indirect-indirect” memory (Cofer, 1967).  Put another way, subjects deliberately intend to consciously recall past events, while priming occurs incidentally when the subject is engaged with some other kind of task.  It should be understood, though, that the direct-indirect distinction applies to memory tests and not to expressions of memory.  In principle, priming could be used to assess consciously accessible memories that the subject declines to report, much as psychophysiological measures are used in forensic lie-detection.  Similarly, a conscious memory could emerge spontaneously in the course of a priming test – a situation that has been referred to as “involuntary explicit memory”.  Moreover, conscious recollection can occur incidentally, as in flashbacks of traumatic memory when some aspect of a task reminds the subject of a past event (Berntsen, 1996, 2009).  In the final analysis, both the “direct-indirect” and “intentional-incidental” dichotomies fail to capture the essence of the explicit-implicit distinction – which is that explicit memory is conscious recollection, and implicit memory is unconscious memory, of the past. 

 

Theories of Explicit and Implicit Memory

            That explicit and implicit memory are dissociable – by various forms of amnesia, by experimental manipulations, and in neuroimaging studies – is now widely accepted.  A variety of theoretical accounts have been offered to explain these dissociations, which boil down to two basic categories: multiple memory systems and multiple memory processes.

 

Multiple Memory Systems

Based on the “modularity” view popular in cognitive neuroscience (Fodor, 1983), a number of theorists have suggested that explicit and implicit memory reflect the performance of separate memory systems in the brain (Schacter & Tulving, 1994b; Schacter & Wagner, 1999; Schacter, Wagner, & Buckner, 2000; Squire, 2004; Squire & Zola-Morgan, 1997).  For example, Squire has identified the neural substrate of the “declarative” memory system with the medial temporal-lobe, including the hippocampus and related structures (Squire & Zola-Morgan, 1991), and the diencephalon.  Damage to the declarative system will impair explicit memory for facts and events but spare implicit memory, which is mediated by other, “nondeclarative”, memory systems.  There are at least five of these, mediating: procedural memory for skills and habits, located in the striatum; priming and perceptual learning, located in the neocortex; simple classical conditioning, located in the amygdala (for emotional responses) and cerebellum (for skeletal responses) and nonassociative learning, located in various reflex pathways.   


Schacter and his colleagues agree that the encoding and retrieval of explicit episodic memories is mediated by the medial temporal lobe system, while various forms of implicit memory are mediated by systems located in the cerebral cortex.  Repetition priming is mediated by a set of perceptual representation subsystems that store representations of the physical structure of the prime, but not its meaning (Tulving & Schacter, 1990).  Semantic priming, as well as the explicit retrieval of semantic knowledge, is mediated by a separate semantic memory system tied to the prefrontal cortex; procedural knowledge is also cortical in nature (Schacter et al., 2000).  They also identify working memory with different cortical centers supporting each of its various components (Baddeley, 2012). 


The relational memory theory of Eichenbaum and Cohen (Cohen & Eichenbaum, 1993; Eichenbaum, 2008; Eichenbaum & Cohen, 2001) is an elaboration of Cohen and Squire’s original distinction between declarative and procedural memory (Cohen & Squire, 1980).  On this account, declarative memory is not exactly synonymous with explicit memory; rather, the hippocampal system is critical for all forms of memory that relate arbitrary or accidental relations between the constituent features of an event – regardless of conscious awareness.  By contrast, a hippocampus-independent procedural system supports the tuning or modification of processing modules engaged during initial learning.  These processing modules are not dedicated to memory per se, but rather reflect plasticity within modules dedicated to perceptual, motor, and other functions. 


Yet another take on the multiple-systems view is provided by Bowers and Marsolek (Bowers & Marsolek, 2003).  Instead of invoking multiple memory systems, they propose that implicit memory is a byproduct of brain systems that are devoted to perceptual pattern recognition, conceptual processing, and motor behavior, rather than memory per se.  On their view, implicit memory is a byproduct of the learning capability of these systems.  These systems have individual memories, in that they are capable of encoding and recognizing information, but they are not memory systems. 


Although Bowers and Marsolek’s approach is based on contemporary theories of object recognition, psycholinguistics, and concept formation, it has its deeper roots in a proposal by Ewald Hering, the 19th-century sensory physiologist, that memory is “a universal function of all organized matter” (Hering, 1870/1880, p. 63).  Hering’s ideas, in turn, were promoted by Samuel Butler, author of Erewhon and The Way of All Flesh, in a ground-breaking book on Unconscious Memory that actually predated Ebbinghaus (Butler, 1880/1910).  Unconscious memory, on Hering’s and Butler’s view, may be likened to the “memory” of a paper clip – which, when once bent, is easier to bend again in the same direction.  Paper clips do not have memory systems, but they do have a physical structure that allow them to retain traces of stimulation.  Bowers and Marsolek do not have much to say about explicit memory, which presumably is mediated by a dedicated brain system.


The multiple memory systems view has been very attractive, not least because something like the doctrine of modularity lies at the heart of contemporary cognitive neuroscience.  Dissociations, whether between explicit and implicit memory or any other measures, are readily explained by postulating separate brain modules underlying performance on each task.  The downside, however, is that it can be tempting to invoke a new brain system whenever we encounter a new dissociation.  Based on studies of verbal repetition priming, for example, some theorists postulated the existence of a visual word form system, associated with the extrastriate cortex, which mediates visual stem-completion, and an auditory word-form system mediating auditory perceptual identification (Schacter & Tulving, 1994a).  However, it is extremely unlikely that a word-form system actually exists in the brain, for the simple reason that writing is only about 5,000 years old – not enough time for the brain to have evolved such a system.  More likely, the perceptual processing of words is mediated by a more generic system which mediates the identification and classification of familiar visual stimuli of all sorts – not just reading (Changeux & Dehaene, 1989; Dehaene & Cohen, 2011).  For this reason, the challenge for multiple-systems theories is to develop a set of principles that would tell us when to stop making such inferences. 

 

Unitary System Theories

By contrast with the multiple-systems view, other theories hold that explicit and implicit expressions of memory are the products of a single memory system.  Perhaps the most intuitively appealing of these is the activation view, which has its roots in generic associative network models of memory.  For example, Rozin suggested that, once encoded, a node in a network retained some residual activation for a period of time – an amount sufficient to support priming, if not conscious recollection (Rozin, 1976).  A more elaborate version was proposed by Mandler, who argued that priming in all its forms is mediated by the automatic activation and integration, at the time of encoding, of pre-existing knowledge structures corresponding to the prime; explicit memory, by contrast, requires effortful elaboration to establish new relations among activated structures (Graf & Mandler, 1984; Mandler, 1980).  But activation, integration, and elaboration all take place within a single memory system. 


Roediger’s transfer-appropriate processing view (Roediger & McDermott, 1993) holds that most implicit memory tasks, such as repetition priming, are “perceptually driven”, in that they require access only to surface features of an object; by contrast, explicit memory tasks are typically “conceptually driven”, in that they require access to semantic or contextual information associated with the studied item.  In this view, dissociations occur because explicit memory depends on “top-down” or “symbolic” processing, while implicit memory depends on “bottom-up” or “data-driven” processing. 


Yet a third single-systems view invokes Jacoby’s process dissociation framework (Jacoby, 1991).  In this view, explicit memory is largely a product of conscious, controlled, effortful, deliberate processing, while implicit memory is largely a product of unconscious, automatic, effortless, involuntary processing.  Jacoby has further introduced a method, the process dissociation procedure, which measures the relative contributions of automatic and controlled processing to any task by pitting them against each other in the “method of opposition”.  A typical result of the PDP is to confirm that the performance of normal subjects on a memory task is mediated by a mix of controlled and automatic processes, while the performance of amnesic patients is largely supported by automatic processes.  One implication of Jacoby’s theory is that explicit memory is a product of controlled processing while implicit memory is a product of automatic processing; but both processes operate within the same memory system.


In some sense, it might seem that implicit memories are simply “weak” memories – too weak to be consciously remembered, but strong enough to give rise to priming effects.  Shanks and his colleagues have offered two different variations on this theme.  The first was based on a connectionist model of memory -- itself perhaps the epitome of a unitary memory model (Kinder & Shanks, 2001; Kinder & Shanks, 2003).  Simulating amnesia by imposing a slower rate of learning, the model predicts that amnesia will affect recognition more than priming.  An alternative computational model, based on signal-detection theory, holds that the same memory underlies both explicit and implicit performance, but that the two tasks differ in terms of the distribution of noise in which the signal is embedded – greater for priming than for recognition (Berry, Shanks, & Henson, 2008).  The model predicts that conditions that affect overall memory strength (like amnesia or deep processing) will be more likely to affect recognition than priming.  Both models, then, yielded exactly the sort of dissociation that gave rise to the distinction between explicit and implicit memory in the first place – without assuming multiple memory systems.


Reder and her colleagues have also argued that explicit and implicit memory draw on the same stored representation (Reder et al., 2009).  In their view, explicit memory requires the formation of new associations, such as between a representation of the item and a representation of the episodic context in which it was presented (see also Kihlstrom, 1997a).  In most priming tasks, however, there is no such new association – the individual item, such as the word doctor, simply stands alone.  Reder’s argument is especially powerful because it is implemented in a general-purpose computational model of memory and cognition which predicts not only a wide variety of explicit-implicit dissociations, involving amnesia, experimental manipulations, and brain-imaging, but also predicts the circumstances under which such dissociations will not be observed.  So, for example, the model predicts that hippocampal amnesia will impair not only explicit recollection but implicit memory for new associations as well as semantic priming, because all require the formation of associations between prime and target; however, hippocampal amnesia will not affect repetition priming, which involves only individual items (Chun, 2005; Wang, Lazzara, Ranganath, Knight, & Yonelinas, 2010).  The theory has the extra advantage of being congruent with recent reinterpretations of the functional role of the hippocampus itself, which is to support processing of the relations among elements in a memory (Eichenbaum, 2003, 2008; Eichenbaum & Cohen, 2001).  In Reder’s view, the difference between explicit and implicit memory is not that one is conscious and the other unconscious, but that one is relational and the other one typically is not.

 

Hybrid Theories

            Thesis, antithesis, and synthesis: naturally, some theorists have proposed models that attempt to combine the virtues of the multiple- and unitary-memory theories.  The easiest way to reconcile these two viewpoints is to propose that different expressions of memory reflect different processes, rather than different memory systems, but that these processes are themselves, mediated by different brain systems.  For example, Henke has proposed that separate brain systems support three different processing modes (Henke, 2010).  These are: rapid encoding of flexible associations (involving the hippocampus and neocortex), slow encoding of rigid associations (basal ganglia, cerebellum, and neocortex), and rapid encoding of single or unitized items (parahippocampal cortex and neocortex).  Like the relational memory theory that inspired it, Henke argues that hippocampal processing need not involve conscious awareness.  Although none of these systems is expressly identified with implicit memory, damage to the hippocampus but not to the parahippocampal cortex and neocortex will impair episodic memory but spare repetition priming – the very dissociation classically observed in the amnesic syndrome. 


            By contrast, Moscovitch and his colleagues have suggested that memory is governed by a very large number of processing components, each associated with a different brain region (Cabeza & Moscovitch, 2013; Moscovitch, 1992).  For example, they argue that the hippocampus supports flexible relational processing involved in both conscious recollection and priming, so long as the priming involves semantic or other relations between representations.  In a similar vein, the ventral parietal cortex supports bottom-up attention involved in episodic memory retrieval.  With such a proliferation of processing components, the component-process framework can account for virtually any pattern of task associations and dissociations that research might discover – an asset that is also a liability.  Cabeza and Moscovitch agree that this approach lacks the appearance of parsimony, but also argue that it makes predictions that are both strong and falsifiable.

 

Testing the Theories

Each of these views has its strengths and weaknesses, not least because they evolved in different research contexts.  Multiple-systems theories are based largely on work with neurological patients, while single-system theories emerged mostly from work on neurologically intact subjects.  The multiple-systems views bask in the reflected glory of cognitive neuroscience, but are bedeviled by the temptation to invoke a new memory system to explain every new dissociation revealed by research.  The activation view gives a plausible account of priming results, but finds it difficult to explain how activation could persist for days or months – as it is sometimes observed to do (Squire, Shimamura, & Graf, 1987; Tulving, Hayman, & Macdonald, 1991).  The transfer-appropriate processing view can explain dissociations not only between explicit and implicit memory, but also those that occur between two explicit or two implicit memory tasks (e.g., one perceptual, the other conceptual in nature; Blaxton, 1989), but has some difficulty explaining dissociations between semantic priming and explicit memory, both of which are, in its terms, conceptually driven.  A further question is whether it is appropriate to term explicit memory as conceptually driven in the first place.


The PDP view, for its part, offers a way to reconcile single-system and multiple-system views: on the assumption that automatic and controlled processes are mediated by separate processing modules that operate on a single memory store.  At the very least, it has provided an increasingly popular technique for measuring the contributions of automatic and controlled processes to task performance.  Like the hybrid theories just described, it offers a way to reconcile single-system and multiple-system views.  However, the mathematics of the PDP requires the troubling assumption that these processes are independent of each other.  An alternative view, also consistent with a single-system view of memory, describes automatic processes as embedded in, and thus redundant with, controlled ones (Joordens & Merikle, 1993; Curran & Hintzman, 1995; Joordens & Merikle, 1993). 


One area where the various theories make competing predictions is with respect to implicit memory for novel, unfamiliar information.  Activation theories would seem to suggest that this is not possible, because there is – by definition – no pre-existing knowledge structure stored in memory to be activated, or modified, by perceptual input.  By contrast, the multiple-systems views are, at least in principle, open to the acquisition of new information.  In fact, there is considerable evidence for priming of novel nonverbal items such as dot patterns and novel objects (e.g., Musen & Squire, 1992; Schacter, Cooper, & Treadwel, 1993) – though not, apparently, for line drawings of “impossible” objects that cannot exist in three-dimensional space (much like the drawings of the Swiss artist M.C. Escher; Schacter, 1990).  Although interpretation of these findings remains somewhat controversial (Ratcliff & McKoon, 1996), priming for novel stimuli would appear to support the multiple-systems view that repetition priming is the product of a perceptual representation system that encodes and preserves structural descriptions of stimulus events.  Priming does not occur for impossible objects because the perceptual representation system cannot form a structural description of objects that cannot exist in three-dimensional space. 


The situation with respect to priming for verbal materials, such as words, is more complicated.  Early results, which showed priming for words like candy and number (which have pre-existing representations in semantic memory) but not for pseudowords like canber and numdy (which do not) are, of course consistent with the activation view of implicit memory (Diamond & Rozin, 1984).  Bowers found priming for words (like kite), nonwords that followed the rules of English orthography (like kers) and for illegal nonwords (like xyks), again contradicting the activation view (Bowers, 1994).  However, as Bowers himself noted, the priming he obtained for illegal nonwords may have been contaminated by explicit memory, which softens the blow somewhat.  On the other hand, Dorfman found  priming for pseudowords made up of familiar morphemes (like genvive) and familiar syllables (like fasney), but not for pseudosyllabic pseudowords (like erktofe) made up of elements that are neither morphemes nor syllables in English (Dorfman, 1994, 1999).  These results are consistent with the view that priming of novel (and familiar) words results from the activation and integration of pre-existing sublexical components stored in memory: priming cannot not occur where there are no such components to be activated.


The failure to find an effect for impossible objects may suggest that activation of prior knowledge contributes to priming of a novel stimulus.  Indeed, in the verbal domain, Stark and McClelland (2000) found a strong repetition effect for words (e.g., bond) and pseudowords that followed the rules of English orthography (e.g., corm); priming of nonwords composed of random consonants (e.g., bdxj) yielded much weaker priming.  This study is noteworthy because the paradigm permitted assessment of priming in the absence of conscious recognition -- ruling out the contamination by explicit memory that has compromised interpretation of prior studies of nonwword and novel object priming.  Further adjudication between activation and acquisition theories may come from neuroimaging studies, as a decrease in neural activity: a decrease in activation during retrieval may reflect activation of pre-existing knowledge, whereas an increase would seem to implicate the acquisition of new knowledge (Henson, 2003). 


The theoretical debate continues back-and-forth, but theoretical development is hampered by the fact that experimental research on implicit memory is almost exclusively focused on a single experimental paradigm – namely, repetition priming.  Roediger and McDermott once estimated that some 80% of implicit memory tests are perceptual in nature, involving variants on repetition priming, about 10% conceptual, and the remaining 10% procedural, and the situation has not changed since then (Roediger & McDermott, 1993).  Viewed in this light, it is not surprising to find theorists proposing that implicit memory is the product of a perceptual representation systems, or of perceptually based processing.  But if implicit memory extends to semantic priming, as indeed it does (Barnier et al., 2001; David et al., 2000; Kihlstrom, 1980; Levy et al., 2004), such theories are too limited to account for the phenomenon.  Repetition priming may be independent of depth of processing -- though a more accurate statement would be that it is only relatively independent; Brown & Mitchell, 1994; Challis & Brodbeck, 1992); but this is unlikely to be the case for semantic priming.  Repetition priming may be modality specific – though not hyperspecific (Rajaram & Roediger, 1993); but again, this is unlikely to be the case for semantic priming.  Research on implicit memory must move beyond repetition priming if we are ever to determine its true nature. 

 

Interactions between Explicit and Implicit Memory

            Owing largely to the hegemony of cognitive neuroscience, the most popular theory of implicit memory remains some version of the multiple-systems view.  Even so, claims for a strict separation of these memory systems should not be made too strongly.  If these various memory modules were truly independent of each other, we would expect to see neurological cases where explicit memory is spared and implicit memory impaired.  The reverse, of course, is what is commonly observed in amnesia.  In fact, only one such case has been reported (Gabrieli, Fleischman, Keane, Reminger, & Morrell, 1995; M.M. Keane, Gabrieli, Mapstone, Johnson, & Corkin, 1995; Wagner, Stebbins, Masciari, Fleischman, & Gabrieli, 1998) and its status is uncertain.  The patient in question, known as M.S., had a scotoma secondary to brain surgery.  He performed normally on a recognition test but poorly on a visual test of repetition priming.  However, he showed normal performance on a test of conceptual priming.  His poor visual priming performance may reflect an extensive lesion in occipital cortex, but on the basis of the conceptual priming results it can hardly be said that he lacked implicit memory. 


            Whatever their underlying basis, the interaction between explicit and implicit memory can also be observed in other ways.  Subjects who consciously recognize that the items on a perceptual-identification test (for example) come from a previously studied wordlist may develop a mental set that actually enhances their priming performance – which is why researchers in this area take care to assess “test awareness” in their subjects (Bowers & Schacter, 1990), and why Jacoby’s “process dissociation” procedure has become so popular (Yonelinas & Jacoby, 2012).  Densely amnesic patients are not able to take advantage of explicit memory, of course, but that does not mean that conscious recollection cannot influence priming in other circumstances. 


Moreover, there is considerable evidence that subjects can take strategic advantage of implicit memory to enhance their performance on tests of explicit memory.  Although free recall epitomizes conscious recollection, both Mandler (1980) and Jacoby (1991) have argued that recognition judgments can be mediated by either conscious recollection of the test item, or by a feeling of familiarity that might be based on priming.  If so, then when implicit memory is spared, subjects can strategically capitalize on the priming-based feeling of familiarity to enhance their performance on recognition tests (Mandler, Hamson, & Dorfman, 1990; Yonelinas, Aly, Wang, & Koen, 2010).  We know that, as a rule, recognition is superior to recall in normal subjects and this is also true for neurological patients with the amnesic syndrome (Sullivan & Verfaellie, 1999), depressed patients receiving ECT (Dorfman et al., 1995), demented patients suffering from Alzheimer’s disease (Snodgrass & Corwin, 1988), and normal subjects with posthypnotic amnesia (Kihlstrom, 1997b).  In addition, studies of recollective experience indicate that amnesic recognition is typically accompanied by intuitive feelings of familiarity, rather than full-fledged remembering (Knowlton & Squire, 1995; Verfaellie, Giovanello, & Keane, 2001).


Accordingly, it seems reasonable to suggest that successful recognition in amnesia can be mediated by spared implicit memory, in the form of repetition or semantic priming.  This claim has been vigorously debated by Squire and his colleagues, who insist that priming is inaccessible to conscious awareness, and so cannot serve as a basis for recognition (e.g., Levy et al., 2004).  Despite methodological issues cutting this way and that, studies employing the process-dissociation procedure clearly indicate that, even among amnesic patients, recognition can be mediated by a priming-based feeling of familiarity (Yonelinas, 2001; Yonelinas, Kroll, Dobbins, Lazzara, & Knight, 1998) – as theory suggests they might be, and as the subjects themselves say they are.  It may be that recollection and familiarity are governed by separate memory systems (Aggleton & Brown, 1999); but against a further proliferation of memory systems, it may be more parsimonious to conclude that explicit and implicit memory interact after all (Dew & Cabeza, 2011).

 

The Phenomenal Experience of Remembering

            The role of familiarity in recognition brings us full circle, to the conscious experience of remembering.  In a seminal paper, Tulving distinguished between two different recollective experiences: remembering, or one’s concrete awareness of oneself in the past, and knowing, one’s abstract knowledge of the past (Tulving, 1985).  For Tulving, the remember-know distinction maps onto his earlier distinction between episodic and semantic memory (Tulving, 1972).  The remember-know distinction was further developed by Gardiner, who showed that “remember” judgments were significantly affected by depth of processing, while “know” judgments were not (Gardiner, 1988).  This is not necessarily the functional dissociation we would expect between explicit episodic and semantic memory, both of which are the product of deep processing; but it is just the sort of functional dissociation we would expect to find between explicit memory and priming memory.  For Gardiner, however, the remember-know distinction maps onto Mandler’s distinction between retrieval and familiarity – closer, that is, to the distinction between explicit and implicit memory.  “Remembering” reflects the conscious retrieval of an episode, including a representation of the event, its spatiotemporal context, and the role of the self as agent or patient, stimulus or experiencer (Brown & Fish, 1983; Fillmore, 1968).  Viewed strictly, “knowing” reflects one’s abstract, impersonal knowledge of the past. 


            The remember-know distinction has proved quite valuable in research on memory and amnesia (Yonelinas, 2001; Yonelinas et al., 2010).  However, it now seems that we should make at least a tripartite distinction among three varieties of recollective experience: “remembering”, or conscious retrieval from episodic memory; “knowing”, or conscious retrieval from semantic memory; and “feeling”, or an inference based on a priming-based feeling of familiarity.  There may even be a fourth variety: “believing”, or an inference concerning the past based on other world-knowledge.  All of these may be dissociable, differential impairment in various forms of amnesia, different effects of experimental manipulations, and different patterns of neural activity.  If so, amnesic patients and others with severely impaired autobiographical memory (Palombo, Alain, Soderlund, Khuu, & Levine, 2015) may be able to use these alternative routes to recollect the past. 

 

The Implicit and the Unconscious

            Together with the concept of automaticity, research on implicit memory constituted our first steps toward a revival of interest in unconscious mental life (Kihlstrom, 1987).  Although the psychological unconscious suffered much in the 20th century from taint by Freudian psychoanalysis – one reason why theorists choose to speak of “implicit” memory rather than “unconscious” memory – the concepts and methods employed to study implicit learning and memory have now been extended to other domains, such as perception (Kihlstrom, Barnhardt, & Tataryn, 1992) and even thinking (J. Dorfman, Shames, & Kihlstrom, 1996) – and beyond cognition to emotion (Kihlstrom, Mulvaney, Tobias, & Tobis, 2000) and motivation (Kihlstrom, 2015; McClelland, Koestner, & Weinberger, 1989).  In this way, the study of implicit learning and memory offer a new, non-Freudian perspective on unconscious mental life – and, in turn, on consciousness itself. 


 

Further Reading

Anderson, J. R. (2000). Learning and memory, 2nd Ed.  New York: Wiley.

Crowder, R.H. Principles of learning and memory.  Hillsdale, N.J.: Erlbaum.

Gluck, M.A., Anderson, J.R., & Kosslyn, S.M. (Eds.) (2008).  Memory and mind: A Festschrift for Gordon H. Bower.  New York: Erlbaum.

Kessen, W., Ortony, a., & Craik, F.  (Eds.) (1991). Memories, thoughts, and emotions: Essays in honor of George Mandler.  New York: Psychology Press.

McConkey, J. (Ed.) (1996).  The anatomy of memory.  Oxford: Oxford University Press.

Nairne, J.S.  (2007). The foundations of remembering: Essays in honor of Henry L. Roediger, III.  New York: Psychology Press.

Reder, L.M. (Ed.).  (1996). Implicit memory and metacognition.  Hillsdale, N.J.: Erlbaum.

Roediger, H.L., Nairne, J.S., Neath, I., & Surprenant, A.M. (Eds.) (2001).  The Nature of Remembering: Essays in Honor of Robert G. Crowder.  Washington, D.C.: American Psychological Association.

Tulving, E.  (2000). Memory, consciousness, and the brain: The Talinn Conference.  New York: Psychology Press.

Tulving, E., & Craik, F.I.M. (Eds.) (2000).  Oxford Handbook of Memory.  Oxford: Oxford University Press. 


 

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