A Component Process Model Based on Modules and Central Systems

Memory and Working-with-Memory: A Component Process Model Based on Modules and Central Systems

Morris Moscovitch Department of Psychology Erindale College, University of Toronto and The Rotman Research Institute Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/4/3/257/1755001/jocn.1992.4.3.257.pdf by guest on 18 May 2021 North York, Ontario Downloaded from http://direct.mit.edu/jocn/article-pdf/4/3/257/1932201/jocn.1992.4.3.257.pdf by guest on 02 October 2021 Abstract A neuropsychological model of memory is proposed that ory that are associativekue dependent, (3) a central system, incorporates Fodor’s (1983) idea of modules and central sys- frontal-lobe component that mediates performance on explicit tems. The model has four essential components: (1) a non- tests that are strategic and on procedural tests that are rule- frontal neocortical component that consists of perceptual (and bound, and (4) a basal ganglia component that mediates per- perhaps interpretative semantic) modules that mediate perfor- formance on sensorimotor, procedural tests of memory. The mance on item-specific, implicit tests of memory, (2)a modular usefulness of the modularkentral system construct is explored medial temporallhippocampal component that mediates en- and evidence from studies of normal, amnesic, agnosic, and coding, storage, and retrieval on explicit, episodic tests of mem- demented people is provided to support the model.

LNTRODUCTION “works with memory” and mediates performance on explicit tests that are strategic.

Memory is not unitary but depends on the operation of MODULES AND CENTRAL SYSTEMS potentially independent, but typically interactive, components. One of the jobs of a cognitive neuropsychologist A distinguishing feature of this memory model is that its is to identify these components and indicate how they basic principles are derived from a consideration of Fo- interact with each other. Although we are far from being dor’s (1983) ideas that modules and central systems are able to specify these components with the precision we the constituents of mind (and brain). Carlo Umilta and would like, either at a functional or structural level, there I, however, proposed a modified version of Fodor’s ideas is sufficient information to tempt many of us to sketch that retained its core assumptions and suggested how the outlines of what we think a complete model might Fodor’s criteria of modularity can be translated to the be like. I offer my version of such a model. neuropsychological level (Moscovitch & Umilta, 1990, The model I sketch has four essential components, 1991). each of which mediates processes that dominate perfor- Modules are computational devices that have propo- mance on four different types of memory tests: (1) a sitional content and that satisfy all of the following three nonfrontal neocortical component that consists of var- criteria: domain specijicity, informational encapsulation ious perceptual and “semantic” modules that mediate or cognitive impenetrability, and shallow output. Do- performance on item-specific, implicit (indirect) tests of main specijicity entails that the type of information mod- memory, (2) a basal ganglia component that mediates ules accept for processing is restricted or circumscribed. performance on sensorimotor procedural tests of mem- At the neuropsychological level, it must be shown that ory, (3) a medial temporaVhippocampa1 component, damage to a particular region or system, the structural which also is modular, and that mediates encoding, stor- embodiment of the module, leads to deficient processing age, and retrieval on explicit (direct) episodic memory in the purported domain with relative sparing of function tests that are associativekue dependent, and (4)a frontal- in other domains. This condition is not sufficient by itself lobe component, which is a central system structure, that since central system structures can also be localized to

0 1992 Mmacbusetts Institute of Technology Journal of Cognitive Neuroscience Volume 4, Number 3 circumscribed regions. Informational encapsulation im- classes of memory tests, explicit and implicit (Graf & plies that modules are resistant to the effects of higher Schacter, 1985). Explicit tests require conscious recollec- order knowledge on processing and are cognitively im- tin of past events whereas on implicit tests, memory for penetrable to probes of their content or operation. Only the past is inferred from changes in performance with the module’s shallow output is available for conscious experience or practice. To be implicit, a test must also inspection. Neuropsychologically, this criterion is satis- be highly structured so that the goal of the task and the fied if the processes mediated by a module are unaffected means to achieve it should be apparent and available to by gross intellectual decline that is caused by degener- the subject (Moscovitch, 1984). When an implicit test ation or focal damage to structures other than the mod- does not meet the latter criteria, the amnesic patient ule itself. For example, patients with generalized shows no evidence of savings even though conscious dementia caused by Alzheimer’s disease fail to under- recollection may not be involved (Nissen, Willingham, & stand even simple words or appreciate the function of Hartman, 1989). objects but they can still read relatively well (Schwartz, Implicit and explicit tests can each be subdivided fur- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/4/3/257/1755001/jocn.1992.4.3.257.pdf by guest on 18 May 2021 Saffran, & Marin, 1980) and have a good three-dimen- ther into at least two subtypes. For implicit tests, the two sional (3D) representation of objects (Chertkow & Bub, are procedural and item speczfic. Procedural tests are 1990; Moscovitch & Umilta, 1990; Warrington & Taylor, those that assess learning and retention of general sen- 1978). The converse also implies informational encap- sorimotor skills, procedures, or rules. Item-specific tests, sulation, namely, a domain-specific deficit with preserved on the other hand, assess memory for a particular item, Downloaded from http://direct.mit.edu/jocn/article-pdf/4/3/257/1932201/jocn.1992.4.3.257.pdf by guest on 02 October 2021 intellectual functions and semantic knowledge about ma- such as a certain word, face, or object by seeing the effect terial in the affected domain. Patients with associative that initial presentation of the item has on accuracy or agnosia may not recognize an object visually but can speed of identification of the item when it is repeated. provide detailed semantic information about the object The benefit gained is known as the repetition priming when given its name. Yet the patient may not be able to effect. use this knowledge to identify the object visually (Mos- The two subtypes of explicit tests are mociativelcue- covitch & Umilta, 1990; Riddoch & Humphreys, 1987). dependent and strategic. Associative episodic memory Shallow ouput is output that has no meaning beyond tests are those in which the cue is sufficient for retrieval. the value assigned to it by the module; interlevel rep- When given the cue “Have you read War and Peace?” or resentations that led to the shallow output are not avail- “Have you seen Gone with the Wind?”the answer auto- able for conscious inspection. The neuropsychological matically pops into mind as surely as the word “night” correlate of this criterion is evidence of normal, domain- pops into mind to the semantic cue “day.” For strategic specific performance without any ability to interpret se- tests, the cue does not elicit the target memory auto- mantically the information pertaining to that domain. matically but provides only the starting point of a mem- Here, too, patients with associative agnosia or dementia ory search that has elements in common with problem- are the paradigmatic cases. Though such patients retain solving. Such strategic processes can be initiated by ques- the ability to process objects, faces, and words at a struc- tions that require the reinstatement of a particular spatial tural, presemantic level, they cannot assign any meaning and temporal context such as “What did you do two to the structural information they have computed (Bauer, weekends ago?” 1984; Chertkow & Bub, 1990; Warrington & Taylor, 1978; There are few, if any tests, that are comprised of only Moscovitch & Umilta, 1990, 1991). a single component. The classificatory scheme suggests Thus, a module, no matter how complex its inner ideal prototypes against which impure tests can be com- workings, is essentially a “stupid,” closed computational pared and thus provides a crude framework for fraction- device that delivers its shallow output to interpretative ating a test into its component parts. central systems where meaning and relevance are assigned. None of the criteria of modularity applies to A NEUROPSYCHOLOGICAL MODEL central systems (but see Moscovitch & Umilta, 1990, for OF MEMORY some provisos). Unlike modules, central systems inte- Input Modules and Item-Specific Implicit grate information from superficially dissimilar domains Tests: Reactivation of Perceptual and and are open to top-down influences. The output of Semantic Records central systems is deep or meaningful and the interlevel representations that give rise to the final output may be Memory begins with the registration of information in available to consciousness. cortical modules that pick up and transform stimulus events into structural, presemantic representations (Fig. 1). The output of these modules is delivered to central CLASSIFICATION OF MEMORY TESTS system structures for early, semantic interpretation. The Task analysis, and evidence of preserved memory abili- input modules and interpretative central systems, which ties in amnesic patients, suggested (Moscovitch, 1984) are presumed to be located in posterior and mid-lateral that it is possible to distinguish between two broad neocortex, are modified by the information they process

258 Journal of Cognitive Neuroscience Volume 4, Number 3 paired by focal lesions or degenerative brain disorders I EVENT I CUE I suggesting that they are mediated by separate modules. r-- Consistent with the principles of modularity, these processes satisfy the criteria of informational encapsulation and shallow output. Demented patients, with degenera- ted central system structures, but spared sensory or para- sensory areas may be able to read and identify object5 at a perceptual level, though they do not know what the words mean or what the objects represent (Schwartz, Saffran, & Marin, 1980; Chertkow & Bub, 1990). Con- versely, if the module (structure) or its output is selectively damaged in nondemented patients, preserved intellectual functions are of little use in making percep- Figure 1. A sketch of the interaction of modules and central system Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/4/3/257/1755001/jocn.1992.4.3.257.pdf by guest on 18 May 2021 structures in a neuropsychological model of memory. (From Mosco- tion fluid. Some of these patients, termed associative vitch, 1989.) agnosics, can recover the perceptual features of the object as indicated by their copies of line drawings and words, but they cannot identify either one. Insofar as thereby leaving, respectively, a perceptual and semantic reading and object identification is possible in these Downloaded from http://direct.mit.edu/jocn/article-pdf/4/3/257/1932201/jocn.1992.4.3.257.pdf by guest on 02 October 2021 record (Kirsner & Dunn, 1985) of their activity. The al- patients, it is a labored, piecemeal, reconstructive process tered neuronal circuitry that underlies the records pre- that often produces erroneous outcomes and bears little serves information about the stimulating event and resemblance to the fluid, almost automatic, and virtually enables subsequently related events to be processed and error-free process associated with normal perception. identified more quickly. Reactivation of perceptual and On implicit rather than explicit tests of knowledge, how- semantic records is the basis for perceptual and concep- ever, such patients perform well, suggesting that the tual repetition priming effects that are at the heart of modules' output has access to nonconscious and nonse- item-specific implicit tests of memory. The term engram mantic procedural systems (Schacter, McAndrews, & is reserved for the informational content of these rec- Moscovitch, 1988). Patients who cannot distinguish fa- ords. miliar from unfamiliar faces explicitly may show a higher In general, the evidence is consistent with the view skin conductance response to familiar faces indicating that input modules mediate performance on perceptual, that their face-recognition module is intact (Bauer, 1984). item-specific tests. In accordance with the criterion of Consistent with our model, patients whose perceptual domain specificity, perceptual repetition priming effects input modules are intact (i.e., who show explicit or im- in normal people are not only modality specific (Tulving plicit identification of the target) also have normal rep- & Schacter, 1990) but also material specific. There is little etition priming effects for words, pictures, and faces transfer from one modality to another, from one repre- (Keane, Gabrieli, Fennema, Growdon, & Corkin, 1991; sentational format (word) to another (picture) (Roediger, Greve & Bauer, 1990; Moscovitch, Winocur, & McLachlan, 1990), and sometimes even from one token to another 1986; Schacter, Rapcsak, Rubens, Tharan, & Laguna, 1990) within the same format if the structural descriptions of if the tests are not contaminated by explicit memory the tokens do not overlap substantially (Cooper, Bied- components (Randolph, 1991). erman, & Hummel, 1992). Repetition priming effects are Perceptual repetition priming effects are stochastically not hyperspecific in the sense that any change in surface and functionally independent of performance on explicit features leads to a reduction of the effects. Rather, rep- tests in normal people (Roediger, 1990; Tulving & Schac- etition priming effects can tolerate changes in surface ter, 1990). This independence is confirmed by striking features such as in font for words and in size, reflection, dissociations between performance on implicit and ex- and foreshortening (if critical features are visible) for plicit tests in brain-damaged patients with material-spe- objects so long as the structurally invariant properties of cific or global amnesia. In such patients, perceptual the stimulus are not altered (Carr, Brown, & Charalam- repetition priming effects can be preserved even though, bous, 1989; Cooper et al., 1992). Semantic variables, such when tested explicitly, the patient's memory for the tar- as the depth to which a target is processed, also have gets and even for the learning episode, is severely im- little influence on the perceptual repetition priming, as paired or absent (Moscovitch, 1982; Shimamura, 1986; would be expected if priming is mediated by input mod- Squire, 1987; Tulving & Schacter, 1990). ules that store information only about structural descriptions (Tulving & Schacter, 1990). Conceptual Repetition Effects Semantic Neuropsychological studies of brain-damaged patients and Records provide the strongest evidence that repetition priming effects are mediated by input modules. Reading, object What distinguishes conceptual from perceptual item-spe- perception, and face recognition can be selectively im- cific tests is that the target is not merely repeated at test

Moscovitch 259 but rather is elicited by semantic cues such as a related apprehended. To the extent that an event does not re- word or a question. Because conceptual repetition prim- ceive full conscious attention, it is not processed by the ing effects, unlike perceptual ones, are influenced by hippocampal component. Using reciprocal pathways that semantic variables, it is unlikely that conceptual repeti- connect the hippocampus to the cortex, the hippocam- tion effects are mediated by presemantic input modules. pus binds or integrates the engrams of the modules and Our suggestion is that they are mediated by a central central systems whose output contributed to the con- system that interprets the shallow-output of perceptual scious experience. The resulting collection of bound modules and stores a semantic record of their activity or engrams constitutes a memory trace that is encoded as representations. Tulving and Schacter (1990) make a sim- a file entry or index within the hippocampal component ilar proposal. (Teyler & Di Scenna, 1986). In accord with the model, conceptual repetition prim- To recollect a recent event consciously, a memory ing effects are reduced or absent in demented patients trace must be reactivated via the hippocampal compo- with Alzheimer’s disease (Butters, Heindel, & Salmon, nent. This occurs when an external or internally gener- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/4/3/257/1755001/jocn.1992.4.3.257.pdf by guest on 18 May 2021 1990). Blaxton (1990) reports a similar pattern of im- ated cue automatically triggers the hippocampal index paired conceptual but preserved perceptual, repetition and interacts with a memory trace, a process called ec- effects in patients with unilateral temporal lobectomies. phory by Semon, who also coined the term engram Because gross intellectual decline is not typical in these (1921, cited in Schacter, Eich, & Tulving, 1978). The patients, her findings, if replicated, would suggest that product of that interaction is delivered to consciousness. Downloaded from http://direct.mit.edu/jocn/article-pdf/4/3/257/1932201/jocn.1992.4.3.257.pdf by guest on 02 October 2021 the anterior, lateral temporal cortex is necessary for stor- Once initiated, ecphoric processes are rapid, obliga- ing semantic records but not for interpreting information tory, informationally encapsulated, and cognitively im- semantically. penetrable. The same is true of the initial formation and Damage to the hippocampal component alone spares encoding of memory traces. We are aware only of the conceptual repetition priming effects. Amnesic patients, input to the hippocampal component and the shallow though severely impaired on explicit tests, can show output from it. Thus, we remember countless daily events normal conceptual repetition effects (Gardner, Boller, without intending to remember them: Memories may Moreines, & Butters, 1973; McAndrews, Glisky, & Schac- “pop”into mind much as preattentive perceptual stimuli ter, 1987; Tulving, Hayman, & Macdonald, 1991), though “pop out” of their background. more studies are needed to confirm the generality of This analogy of memory with perception is appropriate these observations. insofar as aspects of both are modular. Just as it would be maladaptive to have a perceptual system that is too much under our control and subject to our motivations and expectancies, so it would not be useful to have a memory system that relies on our intentions to remem- The Hippocampal Component:A Module for ber. Because most often we do not know in advance what Episodic, Associative Memory will be worth committing to memory, it is important to The hippocampal component consists of a variety of have a system that is capable of encoding and storing structures in the medial temporal lobes and dience- information automatically, as a natural consequence of phalon that form a circuit. In addition to the hippocam- apprehending the material consciously. Moreover, since pus, the structure includes the parahippocampal gyrus, events unfold at their own pace, most of them would not the entorhinal and perirhinal cortices, the mammillary be encoded by the time we could determine that they bodies and dorsomedial nucleus of the thalamus, the were worth remembering. cingulate cortex, and the fornix. Amnesia in humans is The central idea of level of processing theory (Craik associated with bilateral damage to any one of these & Lockhart, 1972) that remembering is a natural by- structures, except for the fornix and cingulate for which product of cognition follows directly from this view of the evidence is equivocal (Squire, 1987). the hippocampal component. Conversely, without a hip- The input modules and central systems deliver their pocampal component, no lasting memory traces can be output to working memory (Baddeley, 1986) whose con- formed and made available to consciousness no matter tent is accessible to consciousness (see Moscovitch & how deeply information is processed (Cermak, 1982). UmiIta, 1990, 1991 for a discussion of working memory An additional benefit of an automatic hippocampal and consciousness) and to procedural systems that can component is that it does not draw cognitive resources affect behavior but whose operation cannot be inspected away from other activities. If committing something to consciously. Information that is consciously apprehended memory always required additional effort beyond that is mandatorily picked up by the hippocampal compo- involved in apprehending the relevant information, it nent. would lead to a peculiar tradeoff-resources allocated The hippocampal component, therefore, is a module to attention and comprehension would be unavailable whose specific domain is information that is consciously for memory and vice versa. We would remember well

260 Journal of Cognitive Neuroscience Volume 4, Number 3 only these items that were processed poorly, an unac- At the neuropsychological level, informational encap- ceptable and counterfactual condition. sulation is satisfied by evidence that dementia does not The cost of being modular is that the hippocampal lead to memory loss if the neuropathology does not affect component lacks the “intelligence” for self-organization, the hippocampal component directly (Neary, Snowdon, strategic intervention, and monitoring. Events are en- Northern, & Goulding, 1988). Conversely, if the hippo- coded only by simple contiguity and by associations that campal system is damaged, elaborative processing at en- memory traces form with each other and with cues. The coding or retrieval will be of limited usefulness in hippocampal component responds reflexively to cues; it improving conscious recollection of recently acquired cannot conduct a memory search if cues are initially information. (Cermak and Reale, 1978; Milner, 1966). ineffective or monitor the ecphoric output to determine Because the hippocampal module accepts, and by im- whether the elicited memories are veridical or even plication, emits semantically coded information, the cri- plausible. The job of organizing the input and verifying terion of shallow output takes on a special meaning when

the output is left to pre- and postecphoric extrahippo- applied to the hippocampal module. The output is shal- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/4/3/257/1755001/jocn.1992.4.3.257.pdf by guest on 18 May 2021 campal processes. Because its organization and retrieval low if the memory is not interpreted properly in relation method is associative, and cue-dependent, we refer to to other memories, that is, if memories cannot be related the hippocampal component as an associative/episodic to a spatial and temporal context with respect to other memory component, a term that also describes the ex- events (Moscovitch & Umilta, 1991). We call this context plicit memory tests mediated by it. organizational in contrast to associative, which refers to Downloaded from http://direct.mit.edu/jocn/article-pdf/4/3/257/1932201/jocn.1992.4.3.257.pdf by guest on 02 October 2021 The specifc domain of the hippocampal component the multimodal spatial and temporal background within consists of consciously accessible information. Informa- which the target is embedded and which comprises an tion that is processed but not delivered to consciousness event. The hippocampus can store information about as a result of brain damage, or information that is not associative, but not organizational, context. Organiza- attended and, therefore, is not apprehended fully in con- tional context is derived from the operation of extrahip- sciousness, will not engage the hippocampal component pocampal central systems on the shallow output of the and will not be remembered on explicit tests (Craik & hippocampal-module. Hippocampally activated memo- Byrd, 1982, and almost any textbook on memory and ries have no temporal organization perhaps with the cognition). exception of that provided by simultaneity or simple In contrast, consciousness as an attribute is irrelevant contiguity. In her novel Moon Tiger, which is concerned to the specific domain of input modules. All that is nec- with the nature of memory and history, Penelope Lively essary for the formation of perceptual records is that puts it this way: “There is no sequence now for those stimuli be picked up by the input modules. Performance days, no chronology. The day is refracted. Hours no on implicit tests gives evidence of memory for poorly- longer linear but assorted like sweets in a jar.”’ attended, unconsciously-perceived information during Dissociations between item and order (Murdock, wakefulness or under light anesthesia even as recall or 1974) or source (Schacter, Harbluk, & McLachlan, 1984) recognition of the same material is, respectively, absent information have been noted in normal people. More or at chance (Kihlstrom, Schacter, Cork, Hurt, & Behr, significantly, patients with focal frontal lesions (Milner, 1990; Merikle & Reingold, 1991). Petrides, & Smith, 1985; Shimamura, Janowsky, & Squire, At the neuropsychological level, domain specificity is 1991) or degenerative disorders that affect the frontal satisfied by evidence that damage to the hippocampal lobes but spare hippocampal components (Vriezen & component produces amnesia on explicit tests without Moscovitch, 1990) have impaired memory for order and concomitant deficits on most implicit tests (Milner, 1966; source but not for items; in contrast, when the hippo- Shimamura, 1986). campal component is damaged but the frontal compo- The hippocampal component is infomationally m- nent is intact, memory for content or items is poor but capsulated in that no other information, except the cue what remains can be ordered normally (Milner et al., itself or information that ultimately evokes that cue, can 1985). lead to recollection of the target item by reinstating the Frontal-lobe damage or dysfunction is an accompany- memory trace. The numerous experiments on encoding ing symptom in almost all cases of confabulation (honest specificity in recognition and recall support this idea lying). Patients who confabulate are informative because (Tulving, 1983). Having studied “cool-grass,’’recognition their behavior suggests what remembering is like when of “grass” is best when “cool” is the retrieval cue. A it relies only on the shallow output from the hippocam- semantically related cue such as “green” may reactivate pal component (Moscovitch, 1989). Confabulations are a semantic record of “grass” but the response will not not usually pure fabrications, but consist of disorganized lead to recollection of it as a target. Importantly, when memories that automatic ecphoric processes deliver to the hippocampal component is damaged, encoding spec- consciousness. Accurately remembered elements of one ificity at the level of conscious recollection is diminished event are combined with those of another without regard or absent (Cermak, 1982; Tulving, 1981). to their internal consistency or even plausibility. Some-

Moscouitcb 261 times entire events are recalled but placed in an inap- with respect to other events, and for using the resulting propriate context. Temporal order is grossly impaired information either to guide further mnemonic searches, even for salient events that are separated by decades. to direct thought or to plan future action. In short, the frontal lobes are necessary for converting remembering from a stupid reflexive act triggered by a cue to an Consolidation us. Recording or Regstration: intelligent, reflective goal-directed activity that is under Remote Memory and the H$pocampus voluntary control. In trying to place a person that looks The term consolidation has traditionally referred to any familiar or to determine where you were during the last process involved in the long-term storage of new infor- week of July, the appropriate memory does not emerge mation. Because the dictionary definition of consolida- automatically but must be ferreted out, often laboriously, tion includes the sense of joining or associating into a by retrieval strategies. unit, and implies that the process may be prolonged, the Memory disorders following frontal lesions are not term should be reserved to describe only the formation related to deficits in storage and retention, which are Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/4/3/257/1755001/jocn.1992.4.3.257.pdf by guest on 18 May 2021 of memory traces by the hippocampus. Recording or hippocampal functions. Instead, they are associated with regfitration should be used to describe the rapid, neo- impaired organizational and strategic processes. As befits cortical process involved in forming records and en- a central system structure for which the criterion of grams. domain specificity does not apply, the frontal lobes’ func- In humans, the consolidation process may take quite tion with respect to memory is similar to its function in Downloaded from http://direct.mit.edu/jocn/article-pdf/4/3/257/1932201/jocn.1992.4.3.257.pdf by guest on 02 October 2021 some time to complete as evidenced by the temporally- other domains. The frontal lobes organize the raw ma- graded retrograde amnesia that accompanies damage to terial that is made available by other modules and central the hippocampal component. Recent memories are the systems. The front lobes’ representations are available to most vulnerable with amnesia diminishing as it extends conscious inspection and the output is deep. If the hip- back in time to a point no earlier than a few months or pocampal circuit can be considered to consist of “raw years (Milner, 1966; Squire & Cohen, 1982). [See Winocur memory” structures, then the frontal lobes are working- (1990) and Zola-Morgan & Squire (1990) for comparable with-memoy structures that operate on the input to the findings in rats and monkeys with hippocampal lesions.] hippocampal component and the output from it. Mos- Once memories are fully consolidated, access to them covitch and Winocur (1992a) prefer this term to the can be gained via an extrahippocampal route perhaps superficially similar working memoy because the latter involving the frontal lobes (Kopelman, 1989). In patients is too theoretically loaded: use of it implies endorsing with Korsakoff ’s syndrome who have frontal dysfunction aspects of a working memory theory in the human and in addition to memory loss, retrograde amnesia may nonhuman literature that are not only incompatible with extend as far back as childhood. each other but may be wrong or inappropriate when applied to frontal lobe functions (Moscovitch & Umilta, i%e Frontal Lobes: Central Systems and Strategic 1990, 1991). Without the frontal lobes, performance on strategic, Explicit Tests explicit, and perhaps some implicit, tests of memory The prefrontal cortex is a large, heterogeneous structure would be impaired (Milner et al., 1985; Moscovitch & consisting of a number of distinct areas, each with its Winocur, 1992b; Petrides, 1989; Schacter, 1987; Shima- own projections to and from other brain regions and mura et al., 1991). These tests include judgment of fre- each having presumably different functions (Pandya & quency of occurrence, self-ordered pointing, conditional Barnes, 1987). It has been appreciated for some time associative learning, different types of delayed response that lesions to the dorsolateral and orbital regions of the that use a small, repeated set of items, and perhaps prefrontal cortex produce different deficits (Milner, release from proactive inhibition (PI). Consistent with 1964). More recently, evidence has been accumulating our hypothesis, the tests are performed poorly not be- that the functions of other, smaller regions, can also be cause the target event is forgotten, as is the case following distinguished one from another (Goldman-Rakic, 1987; hippocampal lesions on the very same tasks, but because Petrides, 1989). organization at encoding and strategic search and mon- Despite the evidence for localization of function itoring at retrieval are deficient in frontal patients. Even among regions of prefrontal cortex, Moscovitch and recall (Incissa della Rochetta, 1986; Mayes, 1988) and Umilta (1990, 1991) argued that they are central system recognition (Delbecq-Derouesnk, Beauvois, & Shallice, structures that contribute to Performance on strategic, 1990) are impaired if strategic processes are involved. explicit tests of memory. The frontal lobes are prototyp- As central system structures, the frontal lobes do not ical organizational structures that are critical for selecting restrict their operation to a specific domain. Memory and implementing encoding strategies that organize the impairment associated with frontal damage is accom- input to the hippocampal component and the output panied by deficits in other domains such as problem from it, for evaluating that shallow output and determin- solving and attention (Miher, 1964; Stuss & Benson, ing its correct temporal sequence and spatial context 1986). The “ordering” deficit on temporal memory tasks

262 Journal of Cognitive Neuroscience Volume 4, Number 3 is also seen when frontal patients recount well-rehearsed version of release from proactive inhibition (PI) and the “scripts” of daily life situations (Godbout and Doyon, California Verbal Learning Test (CVLT). The latter is a test 1992), or reconstruct a motor sequence (Kolb & Milner, of free recall and learning of a 16-item categorized list 1981). Even on memory tests, the strategic impairment that consist of four items from each of four categories. encompasses recent and remote memories (Moscovitch, The list is presented five times and after each time the 1989; Shimamura et al., 1991). subject attempts to recall the items. Normal subjects tend Strategic impairments should extend even to semantic to cluster items by category at recall. In the release from memory. To test this hypothesis, a historical version of PI test, subjects received four different successive lists of the Crovitz test (1973) was devised to supplement the items from the same category (e.g., professions) followed autobiographical version. In the latter, subjects are given by a fifth list from a different category (e.g., sports). Recall a single word, such as “letter” or “broken” and are re- was assessed after each list. quired to relate, in as much detail as possible, an auto- Concurrent interference at study and test, but at nei-

biographical memory related to the target word. In the ther alone, had the predicted effect on both tests: failure Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/4/3/257/1755001/jocn.1992.4.3.257.pdf by guest on 18 May 2021 historical version, subjects were required to describe in to release from PI and lower recall and clustering on all response to words such as “discovery” or “battle” an the trials on the CWT. Not affected by interference were historical event that occurrred before they were born. the number of words recalled on the first trial in release Because the cues do not elicit the appropriate events from PI and the improvement with repetition on the

directly, but require instead an effortful, strategic search, CVLT, both of which are presumed to depend on intact Downloaded from http://direct.mit.edu/jocn/article-pdf/4/3/257/1932201/jocn.1992.4.3.257.pdf by guest on 02 October 2021 we reasoned that patients with frontal lesions or frontal hippocampal functions (Figs. 2 and 3). dysfunction would be impaired on both versions of this Because frontal lobes are central system structures, it test. Amnesic patients without frontal dysfunction were was expected that concurrent interference would also expected to perform well. Data from three patients with affect performance on “frontal” tests in other domains. bilateral frontal lesions and two severely amnesic patients As predicted, sequential finger tapping led to a reduction with intact frontal functions were consistent with these of about 25% on a semantic memory test, letter fluency, predictions. which is sensitive to left frontal damage, but to less than a 5% reduction on category fluency, which is more sensitive to left temporal damage. Cognitive Resources: Cortical Modules, and Although other interpretations of the concurrent in- the Frontal Hippocampal Components and terference studies are possible, the results are encour- Because modules, including the hippocampal compo- aging and support the hypothesis that strategic retrieval nent, process information automatically, they are likely processes mediated by the frontal lobes are resource- to require fewer cognitive resources for their operation demanding whereas ecphoric hippocampal processes re- than would strategic central systems (see Moscovitch & quire less effort by comparison. Umilta, 1990, 1991, on the interaction of central systems with a limited-capacity central processor). Interference by a concurrent task at test should be greater for memory tests sensitive to frontal damage than for tests sensitive to hippocampal damage. (Interference at study may affect both types since it disrupts organization and, if severe Release from PI - nol”l.lien- enough, may prevent information from being fully avail- outprt intsrhnne. Secondary Memory - able to consciousness so that the hippocampus will not - input 1nt.mnne. pick it up.) Consistent with this hypothesis is the obser- I 71 - lnpt and ~Ytpul vation that of the few studies that reported concurrent- Inlehmc. task interference effects at retrieval, almost all used tests that likely were sensitive to frontal damage or dysfunction: verbal fluency (Baddeley, Lewis, Eldridge, & Thompson, 1984), recognition that requires source monitoring (Jacoby, Woloshyn, & Kelley, 1989), and recall of categorized lists (Park, Smith, Dudley, and Lafonza, 1989). To test the retrieval-interference hypothesis directly, we designed experiments that compared the effects of concurrent interference on “hippocampal” tests with those on “frontal” tests. The tests were administered Figure 2. Release from proactive inhibition (PI): Number of words either without interference, or with interference at study, recalled (of a possible 12) by college students per trial in various interference conditions. PI was built up on trials 1-4 and released on at test, or on both occasions. The interfering task was trial 5. The graph only shows words purportedly recalled from sec- sequential finger-tapping (index, ring, middle, small). ond dream memory as calculated by Tulving and Colotla’s 1970 for- The tests we chose were Craik and Birtwistle’s (1971) mula. No PI effects were observed in primary memory.

hfoscovztch 263 normal in amnesic and demented patients with intact sensorimotor structures; and (2) deficits should be ob- Categorized Lists No - served only in patients with sensorimotor-structure dam- (CVLT) - Output interference age, regardless of how preserved their intellect is. - Input interference Both predictions are confirmed by the neuropsychological evidence. Acquisition and retention of sensori- - Input and output motor skills, such as mirror-drawing and pursuit rotor, are normal in the amnesic patient H. M. who had bilateral surgical excision of the medial temporal lobes (Milner, 1966; Corkin, 1968), in patients with lesions to other portions of the hippocampal circuit, and in demented patients with Alzheimer’s disease (Butters, Heindel, &

Salmon, 1990). Learning a general perceptual skill, such Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/4/3/257/1755001/jocn.1992.4.3.257.pdf by guest on 18 May 2021 as reading geometrically transformed script (Butters et al., 1990; Cohen, 1984; Moscovitch et al., 1986) is also 4l preserved in these patients. L 1 2 3 4 5 By contrast, deficits on the same sensorimotor implicit

Trials tests have been noted in patients with Huntington’s or Downloaded from http://direct.mit.edu/jocn/article-pdf/4/3/257/1932201/jocn.1992.4.3.257.pdf by guest on 02 October 2021 Parlunson’s disease, which are degenerative disorders associated with damage to the basal ganglia, structures Figure 3. Recall of categorized lists: Number of words recalled by that are part of the extrapyramidal motor system (Butters college students per trial in various interference conditions. et al., 1990). The same patients, however, perform normally on perceptual, item-specific implicit tests, suggesting that the deficit concerns only the formation of Procedural Implicit Tests sensorimotor records or programs. Of the various types of tests discussed so far, procedural implicit tests are the most heterogeneous, consisting of a large variety of subtypes that do not have obvious Rule-Learning components in common. The tests range from mastering a motor skill (e.g., pursuit-rotor), to acquisition of gen- Amnesic patients can learn and apply mathematical rules, eral perceptual skills (reading geometrically-transformed such as the Fibonacci rule (Kinsbourne & Wood, 1975) script), to learning and applying the rules necessary to or the rules for deriving square roots of two-digit num- solve intellectual puzzles such as the Tower of Hanoi. bers (Charness, Milberg, & Alexander, 1989). Recursive Even classical conditioning of skeletal responses may be rules necessary for solving puzzles such as the various a subtype of procedural implicit tests of memory. To versions of Tower of Hanoi may also be acquired and make the procedural implicit tests more amenable to retained normally by amnesic patients with lesions re- analysis, the term will be used to refer to only two stricted to cortical or diencephalic parts of the hippocam- subtypes: (1) acquisition and retention of sensorimotor pal circuit (Cohen, 1984; Saint-Cyr, Taylor, & Lang, 1988; skills and (2) implicit learning and application of rules. Moscovitch, Osimani, Wortzmann, & Freedman, 1989). Amnesic patients can even learn to write simple computer programs (Glisky, Schacter, & Tulving, 1986). Sensorimotor Skills Implicit derivation and application of rules that require The model we have developed is not directly applicable planning and monitoring of responses are dependent on to the domain of sensorimotor skills because its main the frontal lobes. The Tower of Hanoi is such a goal- concern is with encoding of sensory input. Nonetheless, directed task. Predictably, patients with focal frontal le- the same principle may apply: acquisition and retention sions have difficulty with it (Shallice, 1982), as do patients of slulls results from modification of the very structures with frontal dysfunction that accompanies degenerative involved in performing the task. Just as perceptual struc- diseases of the basal ganglia (Butters et al., 1990; Saint- tures are modified by the act of perceiving to form per- Cyr et al., 1988). The difficulty Korsakoff patients have in ceptual records of their activity, so motor structures solving “Tower” problems is attributable more to their involved in programming are altered to leave behind a impaired frontal-lobe functions than to their amnesia sensorimotor record. Reactivation of sensorimotor rec- (Joyce & Robbins, 1991). Korsakoff patients, however, ords accounts for performance on implicit sensorimotor may not be deficient at learning mathematical rules tests of memory. (Kinsbourne & Wood, 1975) if they did not have to be Two predictions follow from this assertion: (1) Insofar derived and their application provided little opportunity as the tests are truly implicit (Moscovitch, 1984), acqui- to diverge from the goal-directed path (Moscovitch, sition and retention of sensorimotor skills should be 1984).

264 Journal of Cognitive Neuroscience Volume 4, Number 3 independence of Procedural and Item-Spec@c, by grants from the Medical Research Council, the Natural Sci- Implicit Tests ence and Engineering Research Council of Canada, and by a Research Associateship from the Ontario Mental Health Foun- The evidence from studies of patients with neurological dation. disorders indicates that performance on many implicit procedural tests is independent of performance on im- Note plicit, perceptual, or conceptual item-specific tests. Stud- ies of normal people support these conclusions. Using 1. I thank Elana Moscovitch for drawing my attention to the anagram-solving task, McAndrews and Moscovitch relevance of Lively’s book. 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Moscovitch 267