Transcript

The cognitive neuroscience of memory: perspectivesfrom neuroimaging research

DANIEL L. SCHACTER

Department of Psychology, Harvard University, 33 Kirkland Street, Cambridge, MA 02138, USA

SUMMARY

Cognitive neuroscience approaches to memory attempt to elucidate the brain processes and systems thatare involved in di¡erent forms of memory and learning. This paper examines recent research from brain-damaged patients and neuroimaging studies that bears on the distinction between explicit and implicitforms of memory. Explicit memory refers to conscious recollection of previous experiences, whereasimplicit memory refers to the non-conscious e¡ects of past experiences on subsequent performance andbehaviour. Converging evidence suggests that an implicit form of memory known as priming is associatedwith changes in posterior cortical regions that are involved in perceptual processing; some of the sameregions may contribute to explicit memory. The hippocampal formation and prefrontal cortex also playimportant roles in explicit memory. Evidence is presented from recent PET scanning studies that suggeststhat frontal regions are associated with intentional strategic e¡orts to retrieve recent experiences, whereasthe hippocampal formation is associated with some aspect of the actual recollection of an event.

1. INTRODUCTION

Cognitive neuroscience is an interdisciplinary enterprisethat draws on data from studies of brain-damagedpatients, functional neuroimaging techniques, computa-tional models and research with non-human animals(for reviews, see Gazzaniga 1995; Kosslyn & Koenig1992). Cognitive neuroscience approaches to memoryhave grown explosively in recent years. During the pasttwo decades impressive progress has been made in elu-cidating the functional properties of memory and inrelating them to underlying neuroanatomical substrates(for reviews and discussion, see Damasio 1989; Schacter1996; Moscovitch 1994; Squire et al. 1993; Thompson &Krupa 1994)One of the most important new developments in the

cognitive neuroscience of human memory involves theadvent of functional neuroimaging techniques such aspositron emission tomography (PET) and functionalmagnetic resonance imaging (functional MRI). These`windows on the brain' (Posner & Raichle 1994)provide new tools for probing di¡erent aspects ofmemory; they have led to an explosion of recentstudies and a rapid accumulation of novel information(for reviews, see Buckner & Tulving 1995; Ungerleider1995). In this paper I relate ¢ndings and ideas fromneuroimaging studies to an issue that has assumedparamount importance in recent research: the notionthat memory is not a unitary or monolithic entity, butinstead can be fractionated into a number of distinct butinteracting component processes and systems (forreview and discussion, see Schacter & Tulving (1994)).This conclusion has been based largely on converging

evidence from studies of human amnesic patients andlesion studies of experimental animals. I considerrecent neuroimaging research that has begun to illu-minate the nature of the relations among variousmemory processes and systems.

2 . FORMS OF MEMORY ANDFUNCTIONAL NEUROIMAGING

The past two decades worth of research in cognitiveneuroscience have pointed towards a fundamentaldistinction between an explicit or declarative form ofmemory that is critically dependent on the integrity ofmedial temporal lobe and diencephalic brain struc-tures, and an implicit or non-declarative form ofmemory that involves a variety of systems outside themedial temporal/diencephalic region (cf. Eichenbaum1994; Schacter 1987, 1994; Squire 1992; Squire & Zola-Morgan 1991). Explicit memory is re£ected byconscious recall and recognition of recent informationand events. Implicit memory is re£ected by non-conscious e¡ects of past experience on subsequentbehaviour, as expressed by such phenomena aspriming (Tulving & Schacter 1990), skill learning(Cohen & Squire 1980; Salmon & Butters 1995) andhabit formation (Knowlton & Squire 1993; Mishkin1984).While conclusions about brain systems and forms of

memory have relied heavily on research concerninghuman patients and experimental animals with brainlesions, the advent of functional neuroimaging techni-ques provides a new opportunity to map the

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component processes and systems underlying implicitand explicit forms of memory. In studies using PETand functional MRI, estimates of regional cerebralblood £ow are obtained in di¡erent experimentalconditions. Ideally, experimental conditions areconstructed so that they are similar in all respectsexcept for a critical feature that di¡ers between condi-tions. Comparisons are then made between conditionsof interest by subtracting estimates of blood £ow in onecondition from estimates of blood £ow in another. Thelogic of this approach holds that any resulting di¡er-ences in regional cerebral blood £ow are associatedwith the critical feature that distinguishes one condi-tion from another. Because the inferences that onedraws about memory or any other cognitive processesin such a study depends crucially on the speci¢csubtraction that is performed, it is important in PETstudies to hold constant between conditions all vari-ables except for the key parameter of interest (forfurther discussion of the logic of PET studies ofmemory, see Buckner & Tulving (1995)).

3. IMPLICIT AND EXPLICIT MEMORYFOR WORDS : STEM COMPLETION ANDCUED RECALL

An important early PET study of explicit andimplicit memory was reported by Squire et al. (1992).Subjects in Squire et al.'s experiment initially studied alist of familiar words prior to PET scanning (e.g.garden). They were then scanned during a stemcompletion task in which subjects provided the ¢rstword that came to mind in response to three-letterword stems; during one scan stems could be completedwith study list words (priming) and during anotherscan stems could only be completed with new words(baseline). In a separate scan, subjects were given acued recall task in which they were provided withthree-letter stems of study-list words and were asked tothink back to the study list (explicit memory). Thepriming versus baseline comparison revealed decreasedblood £ow in extrastriate occipital cortex. This ¢ndingis important theoretically, because a number of investi-gators have argued that visual word priming dependson posterior cortical regions (Gabrieli et al. 1995;Keane et al. 1995; Schacter 1990, 1994; Squire 1992;Tulving & Schacter 1990). However, Squire et al.(1992) also reported signi¢cant blood £ow increases inthe right hippocampal formation in the priming condi-tion compared to the baseline condition. This ¢ndingwas surprising because previous research with amnesicpatients characterized by medial temporal lobe damagehas shown clearly that such patients typically exhibitnormal priming (for reviews, see Bowers & Schacter1993; Schacter et al. 1993a,c; Squire 1992; Shimamura1986). Based on these ¢ndings, various investigatorshave argued that priming occurs independently of thehippocampal formation (cf. Gabrieli et al. 1995; Keaneet al. 1995; Moscovitch 1994; Schacter 1990, 1994;Squire 1992, 1994). In addition, Squire et al. (1992)observed right parahippocampal gyrus blood £owincreases in the cued recall versus baseline comparison,

implicating the hippocampal region in some aspect ofexplicit recall.Why was the hippocampal region active during

priming in Squire et al.'s (1992) experiment, givenprevious results from amnesic patients indicating thatnormal priming can occur even when the hippocampalformation is damaged? Consideration of Squire et al.'sbehavioural data revealed unusually high levels ofpriming. In fact, the percentage of stems completedwith study list targets in the priming condition (72%)was nearly identical to the percentage of stemcompleted with study list targets in the explicit recallcondition (76%). These ¢ndings raise the possibilitythat priming was c̀ontaminated' by explicit memoryfor study list words. It is known that subjects sometimesexplicitly remember target items on nominally implicitmemory tasks, particularly when the targets are easilyaccessible (cf. Jacoby 1991; Schacter et al. 1989). Consis-tent with this idea, during the study phase of theexperiment, subjects saw all target words twice andperformed a `deep' encoding task (pleasantness rating)that promotes high levels of explicit memory. Becauseshort study lists and brief study-test delays were used,all of these factors operating together may have led tothe evident contamination from explicit memory.Given the theoretical importance of the idea that

priming can occur independently of hippocampal acti-vation, we have recently conducted two PETexperiments that examine issues raised by the Squire etal. ¢ndings (Schacter et al. 1996). Our ¢rst experimentaddressed the possible role of c̀ontamination' fromexplicit memory in the hippocampal activation thatSquire et al. (1992) observed in their priming condition.To evaluate the issue, we conducted an experiment inwhich we used a `shallow' or non-semantic studytasköcounting the number of t-junctions in a wordöin an attempt to eliminate explicit contamination.Previous studies of stem completion priming haveshown that the t-junction counting task can supportrobust priming even when subjects have little or noexplicit memory for the target items (Bowers &Schacter 1990; Graf & Mandler 1984). Accordingly, ifthe priming-related hippocampal activation observedby Squire et al. (1992) re£ects contamination fromexplicit memory, using the t-junction encoding taskshould eliminate both the explicit contamination andthe associated hippocampal blood £ow increases.After carrying out the t-junction task (no scanning

was performed during the encoding task), two separatescans were conducted during which subjects completedthree-letter stems with the ¢rst word that came tomind. One scan consisted of stems that could becompleted with study list words (priming); the otherconsisted of stems that could not be completed withstudy list words (baseline). To maximize the likelihoodof detecting relevant blood £ow changes, the sameseries of non-scanned study list, baseline stem comple-tion and primed stem completionöwhat we call a`study-test unit'öwas carried out three times. Orderof conditions and assignment of items to conditionswas completely counterbalanced.The experiment yielded three key results. First,

analysis of behavioural data indicated that we

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successfully eliminated explicit contamination: theabsolute magnitude of the priming e¡ect was compar-able to priming in previous experiments in whichexplicit contamination could be ruled out (Bowers &Schacter 1990; Graf & Mandler 1984). Also, there wasno indication that priming increased across the threestudy-test units, which would have been expected hadsubjects c̀aught on' to the nature of the experimentand begun to engage in explicit retrieval morefrequently as the experiment progressed. Second, therewas no evidence of blood £ow increases in the vicinityof the hippocampal formation associated with priming.Third, we replicated Squire et al.'s (1992) ¢nding ofdecreased blood £ow in extrastriate occipital cortex inassociation with priming. In addition, we observed avariety of other priming-related blood £ow increasesand decreases (see Schacter et al. (1996), for additional¢ndings, details on PETscanning procedures and othermethodological information).These ¢ndings have potentially important theore-

tical and methodological implications. On thetheoretical side, the data support the position thatperceptual priming occurs independently of the hippo-campal formation. On the methodological side, theSquire et al. (1992) and Schacter et al. (1996) resultsindicate that PET scanning experiments on primingthat use stem completion or similar tasks that areeasily contaminated by explicit memory must also useprocedures that minimize the possibility of explicitcontamination, such as non-semantic study tasks.However, both of these conclusions are compromisedsomewhat by the fact that the failure to observe hippo-campal activity during priming must be viewedcautiously. Negative ¢ndings in PET studies do notcarry the force of positive ¢ndings (e.g. Buckner &Tulving 1995). More importantly, as noted earlier,various studies of explicit retrieval have failed toobserve hippocampal activation (cf. Andreason et al.1995; Shallice et al. 1994; Tulving et al. 1994b). Moreover,in studies that followed-up the initial Squire et al. (1992)¢nding of hippocampal activation during stem cuedrecall (explicit memory), Buckner et al. (1995) failed toobserve hippocampal blood £ow increases whenmodality changed between study and test (i.e. auditorystudy-visual cued recall test) or when the typecase oftarget stimuli changed between study and test (i.e.study words in lower case-test in upper case). If activityin the hippocampal formation is not reliably increasedduring explicit retrieval, then it may not be surprisingthat we failed to detect hippocampal activity duringprimed stem completion performance.In view of these considerations, we performed a

second experiment that examined explicit retrieval onthe stem cued recall test to determine whether wecould observe hippocampal activation. Subjectsstudied a list composed of two di¡erent types of words.Words in the high recall condition appeared four timesand subjects made semantic encoding judgements aboutthem (judging the number of meanings associated witheach word); words in the low recall condition appearedonce and subjects made a non-semantic judgementabout them (judging the number of t-junctions in aword). After seeing study lists in which both types of

words were presented for 5 s each in a random order(no PET scanning was performed during the encodingtask), stem cued recall was tested during separate scansfor high recall words and low recall words. Three suchstudy-test units were carried out to maximize the sensi-tivity of our procedure. The study-test units werepreceded and followed by two separate scans duringwhich subjects were given word stems that could notbe completed with study-list targets and were asked torespond with the ¢rst word that came to mind. Thisbaseline condition provided a control for simpleperceptual, motor and lexical activities.Behavioural data showed, as expected, that subjects

remembered many more words in the high recallcondition (79%) than in the low recall condition(35%). Results revealed clear evidence of blood £owincreases in the hippocampal formation in the highrecall condition, but not in the low recall condition. Inthe high recall minus baseline comparison, we observedbilateral hippocampal activation; in the high recallminus low recall condition, we observed right-sidedhippocampal blood £ow increases. These resultscon¢rm earlier ¢ndings of hippocampal activationduring stem cued recall (Squire et al. 1992). The factthat we observed hippocampal activation during thehigh but not the low recall condition suggests a possiblyimportant distinction regarding the nature of hippo-campal activity during explicit retrieval. Thehippocampal formation does not seem to be activatedby the e¡ort involved in trying to remember a pastevent. In the low recall condition, subjects tried toremember study-list words, but successfully recalledrelatively few of them. Instead, hippocampal activationmay be related to the level or type of recall in a parti-cular situation: some aspect of the actual recollection ofa past event, as opposed to the e¡ort involved inattempting to remember the event. These observationsare consistent with Buckner et al.'s (1995) failure toobserve hippocampal activation in di¡erent modalityand di¡erent case conditions. Although subjects weretrying to recall study list words in both conditions, theway in which they remembered those words may havedi¡ered from the way in which they remembered wordsin the same case condition. For example, their recollec-tions may have been less vivid or less con¢dent in thedi¡erent case or modality conditions compared to thesame case condition. Consistent with these suggestions,our ¢ndings are further supported by results fromanother PET study showing that activity in the leftmedial temporal lobe and hippocampal region is posi-tively correlated with level of successful retrieval inindividual subjects (Nyberg et al. 1996).Schacter et al. (1996) also reported that, in contrast to

the hippocampal activations in the high recall condi-tion, prefrontal cortex was selectively activated in thelow recall condition. More speci¢cally, Brodmannareas 10/46 showed bilateral blood £ow increases inthe low recall minus baseline comparison and left-sided increases in the low recall minus high recallcomparison. As noted earlier, these prefrontal regionshave been activated frequently in PETstudies of explicitretrieval. Our data raise the possibility that blood £owincreases in prefrontal cortex during stem-cued recall

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primarily re£ect the e¡ort involved in attempting toremember past events, as opposed to the actual experi-ence of recollection. The fact that right prefrontalactivity was observed in the low recall minus baselinecomparison, but not in the low recall minus highrecall comparison, is also noteworthy. As Tulving andcolleagues have emphasized, right prefrontal regionsappear to be especially involved in explicit retrieval(e.g. Tulving et al. 1994a). Our results suggest that rightprefrontal regions may be speci¢cally implicated inattempting to generate contextual information thatguides episodic or explicit retrieval. The left prefrontalregion, by contrast, may be involved in other aspects ofe¡ortful search, such as generating candidate responsesunder low recall conditions. One curious feature of our¢ndings, however, is that the right prefrontal region didnot show a signi¢cant blood £ow increase in the highrecall minus baseline comparison. We suggested thatthis might have occurred because retrieval was so easyin the high recall condition that we could not detectsigni¢cant blood £ow increases compared to baseline.Consistent with this idea, there were indeed trends forblood £ow increases in right prefrontal cortex in thehigh recall minus baseline comparison, but they failedto reach the statistical threshold set prior to theexperiment.

4 . IMPLICIT AND EXPLICIT MEMORYFOR NOVEL OBJECTS

In a related PETexperiment (Schacter et al. 1995) weexamined implicit and explicit memory for novelobjects using an experimental paradigm that we hadexplored extensively in previous behavioural work (forreview, see Cooper & Schacter 1992). In this paradigm,subjects are ¢rst exposed to line drawings of novelobjects. Some of the objects are structurally possible;they could exist in three-dimensional form. Others arestructurally impossible: they contain local edge andsurface violations that would prohibit them from actu-ally existing in three dimensions. After encoding aseries of possible and impossible objects during thestudy phase of the experiment, priming is assessed onan object decision task: subjects make possible/impos-sible decisions about studied and non-studied objectsthat are £ashed brie£y (e.g. 50^100ms). Explicitmemory is assessed with a recognition test in whichsubjects make yes/no decisions about old and newobjects.Priming on the object decision tests exhibits a number

of consistent characteristics: it is (i) observed forpossible but not for impossible objects; (ii) dependenton encoding the overall shape of an object; (iii) littlea¡ected by semantic encoding operations that enhanceexplicit memory; (iv) preserved in amnesic patientswith explicit memory de¢cits; and (v) insensitive tostudy-to-test changes in size and left/right re£ection ofobjects that impair explicit memory (e.g. Cooper et al.1992; Schacter et al. 1990; Schacter & Cooper 1993;Schacter et al. 1993b). This overall pattern of ¢ndingshas led us to propose that priming depends on a struc-tural description system (Riddoch & Humphreys 1987)that represents information about the global structure of

an object independently of its retinal size and left/rightorientation (for an alternative interpretation, seeRatcli¡ & McKoon 1995; see also, Schacter & Cooper1995).Schacter et al. (1991) noted that numerous lesion

studies and experiments using electrophysiologicalrecordings implicate regions of inferior temporalcortex in the identi¢cation of complex visual stimuli(for reviews, see Plaut & Farah 1990; Tanaka 1993).Studies of animals with lesions to inferior temporalregions suggest that this region participates in the size-and re£ection-invariant representation of global objectstructure. Accordingly, Schacter et al. (1991) speculatedthat priming of, and object decisions about, structurallypossible objects may involve inferior temporal regions.By contrast, Schacter et al. (1991) suggested that explicitrecognition of novel objects depends on an episodicmemory system involving the hippocampus and othermedial temporal lobe structures (e.g. Squire & Zola-Morgan 1991; Squire 1992).The PET study provided a direct test of these ideas.

We used a variant of the usual object decision/recogni-tion paradigm to accommodate the requirements ofPETscanning. During each of the ¢rst two one-minutescans, subjects saw a series of either 20 possible or 20impossible objects for 50 ms each, and pushed a buttonwhen an object disappeared from the screen. Thepurpose of this no-decision baseline condition was tocontrol for visual stimulation and movement. Subjectsnext studied 20 possible and 20 impossible objects for5 s each in the absence of a scan, and carried out anencoding task that has previously been shown to resultin signi¢cant priming. During each of the next fourscans, subjects made possible/impossible decisionsabout four separate blocks of objects: old possible(possible objects that had appeared on the study list),new possible (possible objects that had not appeared atany previous point in the experiment), old impossibleand new impossible. During the ¢nal four scans,subjects made yes/no recognition decisions about oldpossible, new possible, old impossible and new impos-sible objects. Individual objects were presented for50ms each during each of the eight object decision andrecognition scans.Despite the fact that separating objects into distinct

categories for each scan (e.g. old possible, new impos-sible) constitutes a major departure from the usualprocedure of intermixing di¡erent object types duringtesting, behavioural data in the PET lab were indistin-guishable from previous behavioural data: there waspriming for possible but not impossible objects, andrecognition accuracy was higher for possible thanimpossible objects (Schacter et al. 1995). On the objectdecision task, several key comparisons were made.First, the new object decision minus baseline compar-ison allowed us to examine which brain regions areespecially active when people focus on the globalshape of an object by making a possible/impossibledecision, relative to when they simply look at theobject. According to the ideas outlined earlier, wewould expect to see blood £ow increases in inferiortemporal regions during this comparison for possibleobjects, which have a globally coherent structure, but

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not for impossible objects, which do not. Second, in theold object decision minus new object decision compar-ison, the task is held constant and only prior exposureto the object varies. Therefore, in this comparison wewould expect to see blood £ow changes in brain regionsthat are associated with priming, which, according toour hypothesis, should include the inferior temporalregion for possible objects only. Finally, in the old objectdecision minus baseline comparison, activity relatedboth to priming and object decisions should be evident,so once again we expected to see changes in inferiortemporal regions for possible but not impossible objects.Our hypotheses were supported: analysis of PET datarevealed signi¢cant blood £ow increases in inferiortemporal/fusiform regions for possible objects duringeach of the three preceding comparisons, together withno corresponding increases for impossible objects.On the recognition test, our main interest centred on

the old minus new recognition comparison, in which thetask is held constant (subjects try to remember whetherthey have seen an object in each condition), but subjectsrecollect more objects in the old than in the new recog-nition condition. Here we found blood £ow increases inthe right parahippocampal gyrus for possible objectsbut not for impossible objects. Because possible objectswere remembered more accurately than impossibleobjects, this ¢nding provides a nice parallel to theresults discussed earlier in the high versus low recallprocedure. Again, the evidence suggests that activationof the hippocampal formation during retrieval is relatedto the level or type of recollection. Pertinent informa-tion is also provided by the new recognition minusbaseline comparison. Here, subjects try to rememberwhether an object appeared previously on the studylist. However, because all of the objects are new, subjectscannot `remember'any items from the study list. In thiscomparison, then, subjects are making e¡orts toremember but are not retrieving episodic memories.Here we found blood £ow increases in prefrontal cortexbilaterally for both possible and impossible objects,which probably re£ects retrieval e¡ort. Interestingly,however, we also observed activations in the left hippo-campal formation for both possible and impossibleobjects. These blood £ow increases do not re£ectepisodic memory for previously studied objects. Onepossibility is that they re£ect retrieval e¡ort, in contrastto our ¢ndings from the high versus low recall proce-dure. Another possibility is that they re£ect encodingof the novel or unusual features of our objects. Previousexperiments have shown blood £ow increases in thehippocampal formation during encoding of novelpictures (e.g.Tulving et al. 1994c).In summary, the results of the object memory study

converge with the results of the high/low verbal recallstudy insofar as both studies revealed hippocampalactivation in conditions that yielded high levels ofepisodic memory (high recall, possible objects) relativeto conditions that yielded lower levels of episodicmemory (low recall, impossible objects). In addition,both studies yielded evidence of prefrontal activationsin association with retrieval e¡ort or attempt.Both studies also implicated extrastriate visual cortex

in verbal and non-verbal priming, respectively.

However, whereas priming was accompanied by blood£ow decreases in the word stem completion study, itwas accompanied by blood £ow increases in the objectdecision study. The reasons for these discrepancies arenot entirely clear. One possibility is that blood £owincreases in old object decision minus new object deci-sion comparison are related to some process other thanpriming. For instance, Schacter et al. (1995) pointed outthat more objects are perceived as structurally coherentin the old than the new object decision condition, andthat this di¡erence between the two conditions, asopposed to the process of priming per se, could haveproduced inferior temporal blood £ow increases in theold minus new object decision comparison.The ¢nding that stem completion priming was

accompanied by blood £ow decreases suggests that theprocessing of primed stimuli requires less metabolicactivity and possibly fewer neurons than priming ofnon-primed stimuli. This idea also receives supportfrom experiments with non-human primates, showingthat when they passively view stimuli that becomeincreasingly familiar, the responses of some neurons inthe inferior temporal cortex gradually decrease (for areview of these studies, see Desimone et al. 1995). Inter-estingly, Desimone et al. (1995) note that some inferiortemporal neurons show enhanced responses to repeatedstimuli, particularly when monkeys are required toactively respond to the targets items. Analogously, it isconceivable that priming in humans may be accompa-nied by either blood £ow increases or decreases,depending on task demands (see Ungerleider, 1995, fora helpful discussion of priming-related blood £owdecreases in relation to animal studies, and also in rela-tion to blood £ow increases and decreases in skilllearning experiments).

5. CONCLUDING COMMENTS

Functional neuroimaging studies of human memoryare in their infancy, and we are just now beginning toaddress the complex methodological issues surroundingsuch studies, and to consider the nature of the theore-tical inferences that can be drawn from them.However, the early research reviewed in this papersuggests that the neuroimaging approach constitutes avaluable addition to the methods of cognitiveneuroscience. Of course, neuroimaging studies aloneare unlikely to be su¤cient for understanding thecomplex aspects of brain activity that are involved invarious forms of memory. Although neuroimagingexperiments can inform us about which brain regionsare active during the performance of various kinds ofmemory tasks, they cannot indicate which structuresare necessary for task performance. To obtain thislatter kind of information, it is still important to studymemory de¢cits in patients with localized lesions andspeci¢c forms of memory loss, as well as non-humananimals with experimentally induced lesions (cf.Squire 1992; Thompson & Krupa 1994). By combiningresults from brain imaging and lesion studies, it shouldbe possible to attain a broader understanding of thevarious regions and connections that together comprisethe memory systems of the brain.

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REFERENCES

Andreasen, N. C., O'Leary, D. S., Arndt, S. et al. 1995 Short-term and long-term verbal memory: a positron emissiontomography study. Proc. Natn. Acad. Sci. USA 92, 5111^5115.

Bowers, J. S. & Schacter, D. L. 1990 Implicit memory and testawareness. J. Exp. Psychol. Learn. Mem. Cogn 16, 404^416.

Bowers, J. S. & Schacter, D. L. 1993 Priming of novel infor-mation in amnesic patients: issues and data. In Implicitmemory: new directions in cognition, development, and neuropsy-chology (ed. P. Graf & M. E. J. Masson), pp. 303^326. NewYork: Academic Press.

Buckner, R. L., Petersen, S. E., Ojemann, J. G. et al. 1995Functional anatomical studies of explicit and implicitmemory retrieval tasks. J. Neurosci. 15, 12^29.

Buckner, R. L. & Tulving, E. 1995 Neuroimaging studies ofmemory: theory and recent PET results. In Handbook ofneuropsychology, vol. 10 (ed. F. Boller & J. Grafman),pp. 439^466. Amsterdam: Elsevier.

Cohen, N. J. & Squire, L. R. 1980 Preserved learning andretention of pattern analyzing skill in amnesics: dissociationof knowing how and knowing that. Science 210, 207^210.

Cooper, L. A. & Schacter, D. L. 1992 Dissociations betweenstructural and episodic representations of visual objects.Curr. Direc. Psychol. Sci. 1, 141^146.

Cooper, L. A., Schacter, D. L., Ballesteros, S. et al. 1992Priming and recognition of transformed three-dimensionalobjects: e¡ects of size and re£ection. J. Exp. Psychol. Learn.Mem. Cogn 18, 43^57.

Damasio, A.R. 1989 Time-locked multiregional retroactiva-tion: a systems-level proposal for the neural substrates ofrecall and recognition. Cognition 33, 25^62.

Desimone, R., Miller, E. K., Chelazzi, L. et al. 1995 Multiplememory systems in the visual cortex. InThe cognitive neuros-ciences (ed. M. S. Gazzaniga), pp. 475^486 Cambridge,MA: MIT Press.

Eichenbaum, H. 1994 The hippocampal system and declara-tive memory in humans and animals: experimentalanalysis and historical origins. In Memory systems 1994 (ed.D. L. Schacter & E. Tulving), pp. 147^202. Cambridge,MA: MIT Press.

Gabrieli, J. D. E., Fleischman, D. A., Keane, M. M. et al. 1995Double dissociation between memory systems underlyingexplicit and implict memory in the human brain. Psychol.Sci. 6, 76^82.

Gazzaniga, M. (ed.) 1995 The cognitive neurosciences.Cambridge, MA: MIT Press.

Graf, P. & Mandler, G. 1984 Activation makes words moreaccessible, but not necessarily more retrievable. J. VerbalLearn.Verbal Behav. 23, 553^568.

Jacoby, L. L. 1991 A process dissociation framework: separ-ating automatic from intentional uses of memory. J. Mem.Lang. 30, 513^541.

Keane, M. M., Gabrieli, J. D. E., Noland, J. S. et al. 1995Normal perceptual priming of orthographically illegalnonwords in amnesia. J. Int. Neuropsychol. Soc. 5, 425^433.

Knowlton, B. J. & Squire, L. R. 1993 The learning of cate-gories: parallel brain systems for item memory andcategory level knowledge. Science 262, 1747^1749.

Kosslyn, S. M. & Koenig, O. 1992 Wet mind: the new cognitiveneuroscience. NewYork: The Free Press.

Mishkin, M., Malamut, B. & Bachevalier, J. 1984 Memoriesand habits: two neural systems. InNeurobiology of learning andmemory (ed. G. Lynch, J. L. McGaugh & N. M.Weinberger), pp. 65^77. NewYork: Guilford Press.

Moscovitch, M. 1994 Memory and working-with-memory:evaluation of a component process model and comparisonswith othermodels. InMemory systems1994 (ed. D. L. Schacter&E.Tulving), pp. 269^310. Cambridge,MA:MITPress.

Nyberg, L., McIntosh, A. R., Houle, S. et al. 1996 Activationof medial temporal structures during episodic memoryretrieval. Nature 380, 715^717.

Plaut, D. C. & Farah, M. J. 1990 Visual object representation:interpreting neurophysiological data within a computa-tional framework. J. Cogn. Neurosci. 2, 320^343.

Posner, M. I. & Raichle, M. E. 1994 Images of the mind. NewYork: Scienti¢c American Library.

Ratcli¡, R. & McKoon, G. 1995 Bias and explicit memory inpriming of object decisions. J. Exp. Psychol. Learn. Mem. Cogn21, 754^767.

Riddoch, M. J. & Humphreys, G. W. 1987 Visual objectprocessing in optic aphasia: a case of semantic accessagnosia. Cogn. Neuropsychol. 4, 131^186.

Salmon, D. P. & Butters, N. 1995 Neurobiology of skill andhabit learning. Curr. Opin. Neurobiol. 5, 184^190.

Schacter, D. L. 1987 Implicit memory: history and currentstatus. J. Exp. Psychol. Learn. Mem. Cogn 13, 501^518.

Schacter, D. L. 1990 Perceptual representation systems andimplicit memory: toward a resolution of the multiplememory systems debate. Ann. NYAcad. Sci. 608, 543^571.

Schacter, D. L. 1994 Priming and multiple memory systems:perceptual mechanisms of implicit memory. In Memorysystems 1994 (ed. D. L. Schacter & E. Tulving), pp. 244^256. Cambridge, MA: MIT Press.

Schacter, D. L. 1996 Searching for memory: the brain, the mind, andthe past. NewYork: Basic Books.

Schacter, D. L. & Cooper, L. A. 1993 Implicit and explicitmemory for novel visual objects: structure and function. J.Exp. Psychol. Learn. Mem. Cogn 19, 995^1009.

Schacter, D. L. & Cooper, L. A. 1995 Bias in the priming ofobject decisions: logic, assumption, and data. J. Exp. Psychol.Learn. Mem. Cogn 21, 768^776.

Schacter, D. L. & Tulving, E. 1994 What are the memorysystems of 1994? In Memory systems 1994 (ed. D. L.Schacter & E. Tulving), pp. 138. Cambridge, MA: MITPress.

Schacter, D. L., Bowers, J. & Booker, J. 1989 Intention,awareness, and implicit memory: the retrieval intention-ality criterion. In Implicit memory: theoretical issues (ed. S.Lewandowsky, J. C. Dunn & K. Kirsner), pp. 47^69.Hillsdale, NJ: Erlbaum.

Schacter, D. L., Cooper, L. A. & Delaney, S. M. 1990 Implicitmemory for unfamiliar objects depends on access to struc-tural descriptions. J. Exp. Psychol. Gen. 119, 5^24.

Schacter, D. L., Chiu, C. Y. P. & Ochsner, K. N. 1993aImplicit memory: a selective review. A. Rev. Neurosci. 16,159^182.

Schacter, D. L., Cooper, L. A. & Treadwell, J. 1993bPreserved priming of novel objects across size transforma-tion in amnesic patients. Psychol. Sci. 4, 331^335.

Schacter, D. L., Alpert, N. M., Savage, C. R. et al. 1996Conscious recollection and the human hippocampal forma-tion: evidence from positron emission tomography. Proc.Natn. Acad. Sci. USA 93, 321^325.

Schacter, D. L., Cooper, L. A., Tharan, M. et al. 1991Preserved priming of novel objects in patients withmemory disorders. J. Cogn. Neurosci. 3, 118^131.

Schacter, D. L., Kihlstrom, J. F., Kaszniak, A.W. et al. 1993cPreserved and impaired memory functions in elderlyadults. In Adult information processing: limits on loss (ed. J.Cerella, W. Hoyer, J. Rybash & M. Commons) pp. 327^350. NewYork: Academic Press.

Schacter, D. L., Reiman, E., Uecker, A. et al. 1995 Brainregions associated with retrieval of structurally coherentvisual information. Nature 376, 587^590.

Shallice, T., Fletcher, P., Frith, C. D. et al. 1994 Brain regionsassociated with acquisition and retrieval of verbal episodicmemory. Nature 368, 633^635.

Shimamura, A. P. 1986 Priming e¡ects in amnesia: evidencefor a dissociable memory function. Q. J. Exp. Psychol. A 38,619^644.

Squire, L. R. 1992 Memory and the hippocampus: a synthesisfrom ¢ndings with rats, monkeys, and humans. Psychol. Rev.99, 195^231.

1694 D. L. Schacter The cognitive neuroscience of memory

Phil.Trans. R. Soc. Lond. B (1997)

Squire, L. R. 1994 Declarative and nondeclarative memory:multiple brain systems supporting learning and memory.In Memory systems 1994 (ed. D. L. Schacter & E. Tulving),pp. 203^231. Cambridge, MA: MIT Press.

Squire, L. R. & Zola-Morgan, M. 1991 The medial temporallobe memory system. Science 253, 1380^1386.

Squire, L. R., Knowlton, B. & Musen, G. 1993 The structureand organization of memory. A. Rev. Psychol. 44, 453^495.

Squire, L. R., Ojemann, J. G., Miezin, F. M. et al. 1992Activation of the hippocampus in normal humans: a func-tional anatomical study of memory. Proc. Natn. Acad. Sci.USA 89, 1837^1841.

Tanaka, K. 1993 Neuronal mechanisms of object recognition.Science 262, 685^688.

Thompson, R. F.&Krupa,D. J.1994Organization ofmemorytraces in themammalianbrain.A.Rev.Neurosci.17, 519^549.

Tulving, E., Kapur, S., Craik, F. I. M. et al. 1994aHemispheric encoding/retrieval asymmetry in episodicmemory: positron emission tomography ¢ndings. Proc.Natn. Acad. Sci. USA 91, 2016^2020.

Tulving, E., Kapur, S., Markowitsch, H. J. et al. 1994bNeuroanatomical correlates of retrieval in episodicmemory: auditory sentence recognition. Proc. Natn. Acad.Sci. USA 91, 2012^2015.

Tulving, E., Markowitsch, H. J., Kapur, S. et al. 1994c Noveltyencoding networks in the human brain: positron emissiontomography data. Neuroreport 5, 2525^2528.

Tulving, E. & Schacter, D. L. 1990 Priming and humanmemory systems. Science 247, 301^306.

Ungerleider, L. G. 1995 Functional brain imaging studiesof cortical mechanisms for memory. Science 270,760^775.

The cognitive neuroscience of memory D. L. Schacter 1695

Phil.Trans. R. Soc. Lond. B (1997)


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