Multiple inputs to episodic memory: Words tell another story

Multiple Inputs to Episodic Memory: Words Tell Another Story

Kim S. Graham, Karalyn Patterson,Jane Powis, and Joanna DrakeMedical Research Council Cognition

and Brain Sciences Unit

John R. HodgesMedical Research Council Cognition and Brain Sciences

Unit and University of Cambridge

Seven patients with semantic dementia were asked to recall and recognize 10-word lists ofobject-name vocabulary preselected as either still “known” (correct picture naming andword–picture matching) or now “unknown” (incorrect picture naming and word–picturematching) to each individual patient. The patients showed a significant advantage for knownwords in immediate free recall after several learning trials and also in delayed recall andrecognition. The majority of errors of commission for known words were semantic, whereasphonological errors, especially blends of target words, were produced in the unknowncondition. These findings support claims that (a) multiple inputs from semantic and percep-tual systems support episodic memory and (b) success in verbal and nonverbal episodicmemory tasks is differentially dependent on semantic and perceptual information.

Semantic dementia is a neurodegenerative disease asso-ciated with bilateral but typically asymmetrical atrophy ofthe inferolateral temporal neocortex and the temporal pole(Chan et al., 2001; Galton et al., 2001; Hodges, Patterson,Oxbury, & Funnell, 1992; Snowden, Goulding, & Neary,1989; Snowden, Griffiths, & Neary, 1996). The main neu-ropsychological characteristic is a progressive deteriorationof semantic memory, affecting both verbal and nonverbalaspects and all categories of knowledge, including themeanings of words, objects, facts, concepts, and people.Patients with semantic dementia perform poorly on any taskthat requires semantic memory, such as picture naming,generation of concept definitions in response to a picture orthe spoken name of the object, generation of exemplarsfrom a category, word–picture matching, selection of anappropriate color for a black-and-white line drawing of afamiliar object, sound-to-picture matching, sorting of wordsor pictures according to a prespecified criterion (e.g., landanimals vs. birds), and drawing objects or animals frommemory (Bozeat, Lambon Ralph, Garrard, Patterson, &Hodges, 2000; Bozeat et al., 2000; Hodges et al., 1992;Hodges, Patterson, & Tyler, 1994). By contrast, perfor-

mance on tests measuring other cognitive domains, such asvisuospatial ability, working memory, nonverbal problemsolving, or nonsemantic aspects of language processing(phonology and syntax), is remarkably preserved (Graham& Hodges, 1997; Graham, Patterson, & Hodges, 1999;Hodges, Graham, & Patterson, 1995; Hodges et al., 1994;Snowden et al., 1996).

Because semantic dementia is viewed as a relatively“pure” disease in which all observed deficits may be attrib-utable to semantic disruption, it provides researchers inter-ested in human long-term memory with a unique opportu-nity to investigate the impact of semantic deterioration onother cognitive domains (Graham, Simons, Pratt, Patterson,& Hodges, 2000; Patterson, Graham, & Hodges, 1994). Inthis article, we will concentrate on the impact of semanticimpairment on episodic memory. An influential model oflong-term memory proposes that effective encoding of ep-isodic experiences is dependent on the normal functioningof semantic memory (Tulving, 1995; Tulving & Marko-witsch, 1998). According to this model, termedserial, par-allel, and independent (SPI), when people encounter astimulus event or scene, perceptual information aboutthe stimulus is first processed by the semantic system.Subsequently, meaningful information about the perceptualrepresentation is transferred to episodic memory. The infor-mation encoded into episodic memory can only reflect out-put from the semantic system. This view predicts that pro-gressive degradation of semantic memory, as seen in se-mantic dementia, will result in increasingly impoverishedinput to episodic memory and, in turn, to poor performanceon tests that tap the ability to retrieve episodic experiences.

Recent investigations of episodic memory in semanticdementia suggest, however, an alternative account, in whichperceptual information also contributes directly to episodiclearning and can support episodic memory even in thecontext of severely impoverished semantic knowledgeabout test items. The evidence for this view comes fromstudies (Graham et al., 2000; Simons, Graham, Galton,

Kim S. Graham, Karalyn Patterson, Jane Powis, and JoannaDrake, Medical Research Council Cognition and Brain SciencesUnit, Cambridge, England; John R. Hodges, Medical ResearchCouncil Cognition and Brain Sciences Unit and University Neu-rology Unit, Addenbrooke’s Hospital, University of Cambridge,Cambridge, England.

We are immensely grateful to the 7 patients and our controlvolunteers for agreeing to participate in the study. We also thankKatherine Pratt and Jon Simons for help with data collection. Thisresearch was supported by the Medical Research Council (Kim S.Graham, Karalyn Patterson, and John R. Hodges) and by a Well-come Trust Grant (John R. Hodges and Kim S. Graham).

Correspondence concerning this article should be addressed toKim S. Graham, Medical Research Council Cognition and BrainSciences Unit, 15 Chaucer Road, Cambridge, CB2 2EF, England.E-mail: [email protected]

Neuropsychology Copyright 2002 by the American Psychological Association, Inc.2002, Vol. 16, No. 3, 380–389 0894-4105/02/$5.00 DOI: 10.1037//0894-4105.16.3.380

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Patterson, & Hodges, 2001) that contrasted memory foritems in two conditions: (a) perceptually identical: the samepicture was shown at study and test; (b) perceptually dif-ferent: the picture at test depicted the same stimulus objector person as seen at study but displayed either a differentview or a different exemplar of the object (e.g., a touchbutton vs. a round-dial telephone). Furthermore, half of thestimulus items (objects or famous faces) were selected foreach patient to be “unknown,” in the sense that the patientcould no longer name the picture, produce informationabout the object or person depicted, or select it correctlyfrom a set of semantically related foils. Recognition mem-ory performance of the patients with semantic dementia wastypically excellent for the perceptually identical condition,for unknown as well as “known” items. In the perceptuallydifferent condition, recognition success was modulated bythe semantic status of the stimulus concept: good recogni-tion for known items but impaired recognition memory forpictures of previously familiar objects that are no longerknown to the patient (Graham et al., 2000; Simons et al.,2001). These experiments suggest that there are multipleinputs to episodic memory and that perceptual informationabout studied items will—typically in conjunction with buteven in the absence of adequate meaningful input from thesemantic system—support new learning.

Although these experiments clearly demonstrate that ep-isodic memory for pictures does not necessarily depend ona normally functioning semantic system, Graham et al.(2000) noted that this outcome should not be expected tohold true under all circumstances or for all types of stimulusinput. Episodic memory for verbal material presumablyrequires substantially more support from the semantic sys-tem than memory for pictorial stimuli because there is lessperceptual information available from the study episode toaid subsequent discrimination in the test phase. A directprediction from the multiple input view of new learning,therefore, is the following: For patients with semantic de-mentia, even without the additional perceptual manipula-tions required to reveal significant effects of semantic mem-ory status in recognition memory tests for pictures, recog-nition memory for words should yield generally poorperformance and a significant advantage for material thatthe patients still comprehend relatively well.

In a study of one aspect of memory for verbal material insemantic dementia (Graham, Patterson, Pratt, & Hodges,1999), a patient, D. M., was asked to relearn words from anumber of different semantic categories on which he hadpreviously shown profoundly impaired performance whenasked to produce the names of exemplars in a categoryfluency task. Several results from that study are relevant tothe experiment described here: (a) D. M.’s repeated practicewith vocabulary (30 min a day for 2 weeks) improved hisproduction of the names of category exemplars to a levelwell within the range of the control participants tested in thestudy; (b) the extent of D. M.’s improvement in wordproduction seemed to be related to how much prior semanticknowledge he possessed about the categories; and (c) un-usually for D. M., or indeed for any patient with semantic

dementia, he made a number of phonologically relatederrors while attempting to produce exemplars belonging toa category.

At first glance, the success with which D. M. increasedhis vocabulary output might seem to contradict the predic-tion that episodic memory for verbal stimuli should beimpoverished in semantic dementia. Notably, however,D. M. was practicing with materials that frequently includedpictures of concepts, as well as the name of the item, and healso had an unusually high degree of exposure to thesematerials by practicing with them every day over 2 weeks.It seems reasonable to assume that D. M.’s exceptionalperformance reflected these two factors and that if he hadbeen tested after only one or two exposures to the stimuli, hemight have continued to show a significant impairment oncategory fluency. Furthermore, although it was not possibleto test this factor directly in Graham, Patterson, Pratt, andHodges’ (1999) experiment, there was anecdotal evidencethat D. M. showed slightly better learning (and subsequentlyless forgetting) of exemplars from categories for which hehad either richer previous knowledge or repeated exposurein addition to his practice sessions (e.g., names of televisionshows).

The third result from the category fluency relearningexperiment of note here is the fact that D. M. made asignificant number of phonological errors, in particular pho-nological blends between exemplars from the same categorylist (e.g., having practiced items from the category “stonesand gems” that included the exemplars “ topaz” and “opal,”D. M. produced the blend error “opaz” ). Patients withsemantic dementia virtually never make phonological errorsin spontaneous speech or object naming but have beenobserved to make a significant number of such errors inimmediate serial recall of strings of three to four previouslyfamiliar unrelated words that had degraded meanings for thepatient (Knott, Patterson, & Hodges, 1997; Patterson et al.,1994). Patterson et al. (1994) argued that in the normalspeaker, the phonological elements of a familiar word areheld together by two factors resulting from regular co-occurrence: (a) links between the segments in the speechproduction system and (b) links between the semantic andthe phonological representations of a word. In semanticdementia, in which there is a progressive deterioration ofconceptual knowledge, the resulting gradual loss of seman-tic “binding” was hypothesized to yield the blend and trans-position errors under conditions of high phonological load.To explain D. M.’s phonological errors in category fluency,Graham, Patterson, Pratt, and Hodges (1999) proposed thatbecause D. M. always practiced the words within a categoryin a fixed order, for him this task could be consideredequivalent to the serial recall of strings of words. A predic-tion from these studies is therefore that patients with se-mantic dementia should produce phonological errors in averbal recall task for unknown words.

To date, there have been few systematic investigations ofverbal memory in semantic dementia, despite the fact thatexperiments on episodic memory for other kinds of materialin such patients have proved theoretically informative(Graham, Becker, & Hodges, 1997; Graham, Patterson,

381VERBAL MEMORY IN SEMANTIC DEMENTIA

Pratt, & Hodges, 1999; Graham et al., 2000; Simons et al.,2001; Simons, Graham, & Hodges, in press). The followingexperiment was specifically designed to address the follow-ing questions:

1. Would patients with semantic dementia show im-paired episodic memory for verbal material when testedover typical learning time periods?

2. Would there be significant effects of semantic mem-ory status on success in episodic memory tests for words aspredicted by both the multiple input view of long-termmemory (Graham et al., 2000) and the SPI framework(Tulving, 1995)?

3. Would the patients produce phonological errors inverbal recall, particularly for unknown words (i.e., previ-ously familiar words that now have degraded semanticrepresentations for the patient in question)?

Method

Participants

Participants in this study included 7 patients who fulfilled con-sensus criteria for semantic dementia (Hodges et al., 1992; Snow-den et al., 1996) and 20 neurologically healthy control participantswho were members of the Medical Research Council Cognitionand Brain Sciences Unit volunteer panel. The control participantswere matched in terms of age and education to the first 4 patientsrecruited for this study (A. M., S. L., J. H., and G. C. B.), with asubset of 5 control participants per patient: A. M. controls � 64.80years (SD � 1.30), with 16.20 years of education (SD � 0.45);S. L. controls � 51.40 years (SD � 0.89), with 13.40 years ofeducation (SD � 2.41); J. H. controls � 60.60 years (SD � 2.19),with 11.20 years of education (SD � 0.84); and G. C. B. con-trols � 59.60 years (SD � 2.30), with 13.00 years of education

(SD � 1.87). Each subset of control participants received the sameword lists as their matched patient. Analysis of these control datarevealed no significant effects of stimulus selection (which wasdifferent for each patient to take account of semantic status),condition (known vs. unknown items), or age (which spanned 51to 65 years). The sets of items created for the other 3 patients werenot, therefore, tested in controls.

The patients were identified through the Memory DisordersClinic at Addenbrooke’s Hospital, Cambridge, England. All 7patients presented with a history of progressive deterioration ofvocabulary and comprehension. Table 1 shows the performance ofthe patients on a battery of neuropsychological tests, includingpicture naming, category fluency, and word–picture matching fromthe Hodges and Patterson semantic battery (Hodges & Patterson,1995). All 7 patients were significantly impaired on these threesemantic tasks and also on an associative test of semantic knowl-edge, the Pyramid and Palm Trees Test (Howard & Patterson,1992). In terms of other cognitive domains, all 7 patients hadrelatively preserved performance on forward and backward DigitSpan and copying of the Rey Complex Figure (Osterrieth, 1944).The only exception to this was C. S., who managed only 2 onbackward Digit Span and 21/36 on copying of the Rey Figure.C. S. was also unable to recall any details of the Rey Figure aftera delay of 45 min and was at chance on both the words and facesversion of Warrington’s Recognition Memory Test (Warrington,1984). There was variable performance on this standard test ofepisodic recognition memory for the other 6 patients (note thatsome were given the full 50-item version, whereas others per-formed the short 25-item test).

Procedure

The experiment comprised two parts: (a) an initial pretest usingthe Snodgrass and Vanderwart (1980) picture corpus to assess thepatient’s knowledge of object concepts and their names and (b) anexperimental component to assess learning, recall, and recognition

Table 1Performance of Each Patient With Semantic Dementia and 24 Healthy Control Participantson a Battery of Standard Neuropsychological Tests

Tests

Patients Controls

A. T. S. L. M. A. C. S. G. C. B. A. M. J. H. M SD

Age (years) 65 51 62 63 59 65 60 70.0 7.8Education (years) 20 12 13 10 11 16 10 10.8 2.3

Balance of temporal atrophy L � R L � R L � R R � L L � R L � R L � R

MMSE (30) 25 24 29 15 24 8 12 29.2 1.0

Digit Span forward 8 5 6 4 5 5 7 6.8 0.9Digit Span backward 4 4 3 2 4 5 6 4.7 1.2

Rey Copy (36) 36 30 36 21 36 35 34 34.0 2.9Rey, 45-min delay (36) 24.0 14.0 6.5 0 9.0 6.5 7.0 15.3 7.4RMT Faces (25 or 50) NT 0.92 0.78 0.48 0.64 0.54 0.84 0.88 0.80RMT Words (25 or 50) NT 0.84 0.84 0.44 0.78 0.52 0.64 0.94 0.60

Naming (48 or 64) 0.16 0.28 0.20 0.73 0.56 0 0.14 0.91 0.05Category Fluency (8 categories) 17 19 15 38 52 1 16 113.9 12.3WPM (48 or 64) 0.91 0.75 0.89 0.80 0.77 0.27 0.42 0.99 0.02PPT pictures (52) 0.90 0.85 0.79 0.79 0.83 0.67 0.71 0.98 0.03PPT words (52) 0.85 0.73 0.81 0.75 0.61 0.58 0.61 NT NT

Note. Maximum scores are in parentheses after the test name, and the control data (M and SD) are from Hodges and Patterson (1995).Chance performance for the RMT and PPT is 0.50. For WPM, chance is between 0.10 and 0.13. MMSE � Mini-Mental State Examination(Folstein et al., 1975); Rey Figure (Osterrieth, 1944); RMT � Recognition Memory Test (Warrington, 1984); NT � not tested; WPM �Word-Picture Matching (Hodges & Patterson, 1995); PPT � Pyramid and Palm Trees Test (Howard & Patterson, 1992).

382 GRAHAM, PATTERSON, POWIS, DRAKE, AND HODGES

for known and unknown vocabulary. Apart from the addition ofthe known–unknown manipulation, Part B of the experiment wasmodeled on the Consortium to Establish a Register in Alzheimer’sDisease test of verbal learning, recall, and recognition (Welsh,Butters, Hughes, Mohs, & Heyman, 1991).

Initial pretest. Each of the 7 patients was asked to name all260 black-and-white line drawings from the Snodgrass andVanderwart (1980) picture corpus. Approximately a week later,they were given a four-choice word–picture matching test (onespoken word, four semantically related pictures) for the same 260items. On the basis of results from these two assessments, weselected 10 pairs of words (known–unknown) for each patient; thepairs were matched for written word frequency (Kucera & Francis,1967) and syllable length. The known set for each patient consistedof vocabulary corresponding to concepts that he or she was able toname correctly from a line drawing and also to select correctlyfrom other semantically related foils on the word–picture matchingtest. The unknown set comprised words corresponding to conceptsthat the patient failed both to name and to select. For the recog-nition memory component of the test, 10 new pairs of words werechosen to serve as foils for the known and unknown old words.The foil word pairs were matched to each other for semanticcategory (e.g., “attic” and “cellar” ; “ tulip” and “orchid” ), wordfrequency, and syllable length. It should be noted that the status ofthe foil stimuli with respect to each individual patient’s knowledgeof the words was not tested. The proportion of known and un-known foil words, therefore, was not known for each individualpatient.

Experimental task: Patients. The main experiment was con-ducted at a later date, within a few weeks following constructionof the vocabulary sets from the pretest and over two experimentalsessions separated by approximately 1 week. Counterbalancedacross patients, the first session was devoted to either known orunknown words, with the other condition assigned to the secondsession. In each session, the patient was shown his or her 10unknown or known words presented singly on cards and asked toread each word out aloud. Immediately after reading the last wordof the set, the patient was asked to recall as many of the words aspossible in any order. This procedure was repeated another twotimes, using a different word order with each presentation, result-ing in a total of three scores (out of a possible 10) for immediatefree recall. Following a filled delay of 5 to 10 min, the patient wasasked once more to recall as many of the words as possible andwas then given a yes–no recognition memory test comprisingthe 10 target words (in the same order as presented on the firstrecall trial) interspersed with the 10 foil words.

On the few occasions that a patient incorrectly read aloud apresented word, the experimenter provided the correct pronuncia-tion. During recall, an item was scored correct if the patientproduced the same incorrect pronunciation of the word that he orshe had used earlier. In one patient, C. S., all the words had to beread to him.

Experimental task: Controls. The control participants weretested in subsets of 5 controls matched to 1 patient, over twosessions separated by approximately a month. The control volun-teers were presented with the 10-item word lists on a slide pro-jector (2 s per word) and asked to read the words silently. Afterpresentation of the 10th and final word in each set, the controlparticipants were asked to recall in writing as many of the wordsas they could remember in any order on 10 pages in a mini-booklet(1 word per page). This procedure was repeated twice more, usingthe same word orders generated for the patients. Following a filleddelay of 10 min, they were asked to recall as many of the words aspossible, again in any order, in a new booklet. They then per-

formed the yes–no recognition test by circling a y (for yes) or n(for no) on a presented sheet with the 10 words and the 10 foilwords randomly intermixed (in the same order as was given toeach patient). Approximately 1 month later, the control partici-pants were asked to perform the task again with the alternativeword set (either known or unknown for the matched patient). Theorder of the presentation of the known and unknown sets was onceagain counterbalanced.

Results

The data were first analyzed using an analysis of variance(ANOVA) that consisted of two within-subject factors: (a)knowledge: known versus unknown; and (b) experimentalcondition: immediate recall (Trials 1, 2, and 3), delayedrecall, and delayed recognition. There was also a singlebetween-subject factor of group (patients vs. controls). Theanalysis revealed significant main effects of knowledge,task, and group: F(1, 25) � 13.60, p � .01; F(4,100) � 68.70, p � .01; and F(1, 25) � 149.60, p � .01,respectively. Two of the interactions with group were alsosignificant: knowledge, F(1, 25) � 17.90, p � .01; andexperimental condition, F(4, 100) � 9.40, p � .01. Theinteraction between task and knowledge approached signif-icance, F(4, 100) � 2.37, p � .06; but there was noevidence of a three-way interaction.

To investigate whether knowledge was a major determin-ing factor in the patients’ performance, we further analyzedthe data using 2 � 2 mixed measure ANOVAs based ondata from each experimental condition (within factor,knowledge; between factor, group). These analyses revealeda significant main effect of group in all five components ofthe word learning test, F(1, 25) range � 37.9–179.1, p �.01; and planned t tests confirmed that this effect was due topoorer performance in the patients (both for known andunknown vocabulary) compared with controls, t(25)range � 6.0–10.7, p � .01. This deficit is clearly illustratedin Figures 1 and 2. Figure 1 documents the control partic-ipants’ performance in the four recall trials (immediate anddelayed) contrasted with the patients’ recall of known andunknown stimuli. Note that in Figure 1 and in all subsequentfigures, the control data correspond to scores averagedacross the sets of items judged as known and unknown forthe patients, because this variable had (as expected) noimpact on control participants’ performance. Figure 2shows performance on the delayed recognition componentof the test as measured by hits minus false positives.

The ANOVAs also confirmed significant main effects ofknowledge, F(1, 25) range � 4.16–29.8, range p � .05–.01;and Knowledge � Group interactions, F(1, 25) range �4.6–28.0, range p � .05–.01, in four out of five task con-ditions. Paired t tests confirmed significantly better recall ofknown than unknown words at Recall Trial 3, delayedrecall, and delayed recognition, t(6) range � 2.3–3.1, p �.05. Although there were numerical advantages for knowncompared with unknown items at Trials 1 and 2, thesedifferences did not reach significance (see Figure 1).

Notably, despite clearly abnormal performance on thethree immediate recall trials, the patients did show somelearning over repeated presentation of the items: In the


known condition, the patients on average recalled just overtwice as many words by Trial 3 (M � 5.57, SD � 1.80) asthe number produced at Trial 1 (M � 2.70, SD � 1.80).There was also a gain, though from a lower baseline, in theunknown condition, with performance on Trial 1 (M � 2.00,SD � 1.53) increasing only to a mean of 3.57 (SD � 1.9)words by Trial 3.

There was a suggestion that the patients showed greaterforgetting for unknown than known words: As a group, afterthe delay, they retained only 32% of Trial 3 unknown items,as compared with 62% of known words. It is important tonote, however, that the differential levels of performancebetween the two conditions at Trial 3 may reflect poorerinitial learning in the unknown condition, rather than morerapid forgetting during the delay (see Figure 1).

Individual Analyses

The range of performance on all the tasks was extremelyvariable across patients. For example, on the learning trials,performance ranged from one to nine items recalled in theknown condition and one to seven words in the unknowncondition. Furthermore, although some patients demon-strated evidence of learning (e.g., C. S. produced no exem-plars initially in the known condition, but managed five byTrial 3), others did not manage to improve their recall at allover successive learning trials (A. M. recalled three knownitems after each presentation). Figure 3 demonstrates thisvariability in performance across the group by showing the

individual patterns of recall over the three trials for eachpatient’s known (see Figure 3A) and unknown (see Figure3B) words. The patients are ordered on the graph accordingto performance (from best to worst) for known items on therecognition memory task.

At delayed recall (see Figure 3C), 3 patients (A. M., C. S.,and A. T.) were unable to recall any unknown words. In theknown condition, only A. M. showed such disastrous per-formance, and all the other patients produced at least two orthree items from the list.

Recognition memory revealed striking individual differ-ences both in overall level of success and in the impact ofknowledge for these vocabulary items. Figure 4 shows theperformance of the 7 patients on the known and unknownconditions as measured by hits minus false positives. Themost mildly impaired patient (S. L.) displayed perfect rec-ognition memory for both known and unknown words, andat the other end of the spectrum, A. T. was equally impairedin both conditions; but the remaining 5 cases were moresuccessful, sometimes substantially more so, in discriminat-ing known than unknown words from new foils.

Error Analysis

Unlike control participants, 5 of the 7 patients with se-mantic dementia made errors of commission as well asomission on the recall component of the memory task. Toexamine differences in the types of errors across the knownand unknown conditions, we grouped the responses (a totalof 54) into four categories:

1. Semantic (“ lion” for “ tiger” ; or a circumlocution, suchas “great big striped thing in Africa” for “giraffe” );

Figure 2. Recognition memory scores, calculated by subtractingfalse positives from hits, for the control participants (known andunknown averaged) and patients (known and unknown shownseparately). The patients showed significant impairment on bothstimuli types compared with the control group.

Figure 1. Performance of the patients (known and unknownwords are shown separately) and control participants on the fourrecall conditions: immediate (Immed. 1, 2, and 3) and delayed.Note that the control data are based on averaging the scores acrossthe known and unknown vocabulary. Although the patientsshowed similar levels of learning compared with the control par-ticipants across the three immediate recall trials, it is notable thatperformance was significantly impaired in the patients for bothknown and unknown items.


2. Phonological (“ thumble” for “ thimble” ; or blends,such as “ thistle” for “ thimble” and “whistle” );

3. Perseveration (repeat of a target word or error);4. Miscellaneous (where the source of an error was not

clear).

The patients made 23 and 31 errors in the known andunknown conditions, respectively. Figure 5 reveals a nota-

Figure 5. Comparison of the errors made by 5 out of 7 patientswith semantic dementia for known versus unknown words. Themajority of the errors in the known condition were semantic innature, whereas in the unknown condition the errors were predom-inantly phonological.

Figure 3. The performance of each individual patient (repre-sented by his or her initials on the x-axis) on three immediate recalltrials for (A) known and (B) unknown vocabulary. Figure 3Cillustrates performance on both types of experimental stimuli in thedelayed recall condition. The graphs demonstrate that performanceon the recall tasks was quite variable across patients, althoughthere was a clear advantage for recall of known words comparedwith unknown words.

Figure 4. Recognition memory scores were calculated by sub-tracting false positives from hits for each individual patient (rep-resented by his or her initials on the x-axis) and for known versusunknown stimuli. Virtually all the patients showed an advantagefor recognition of stimuli that were still familiar to them comparedwith words that were previously familiar but were no longerknown.


ble difference in the pattern of errors across the known andunknown conditions. Approximately half of the errors in theknown condition were semantic in nature (n � 12), withonly 13% (n � 3) being classified as phonological. Bycontrast, the opposite pattern was seen in the unknowncondition, with more than half of the errors being classifiedas phonological (n � 17) and under 10% (n � 3) of theerrors having a semantic relationship to a target word. Therest of the responses were either perseverations (known �5; unknown � 3) or errors that could not be easily classified(known � 3; unknown � 8).

Serial Position Effects

Serial position data for the patients are somewhat difficultto interpret in an unambiguous way, given that recall per-formance was so poor on Trial 1 and that on Trials 2 and 3,the impact of order of presentation on that trial might beconfounded by the different order(s) of presentation on theprevious one or two trials. Nevertheless, it seems worthnoting (a) that the only strong effect on Trial 1 was adramatic one-item recency effect for the unknown condi-tion, with every single patient recalling his or her last-presented word from this list on the first trial; and (b) thatthe general pattern of serial position effects emerging overthe three trials of immediate free recall for the semanticdementia group appears entirely normal. That is, especiallyfor the known word lists, by Trial 3 the patients showed asmall (typically one-item) primacy effect and a larger re-cency effect extending over the last three to four words.

Discussion

The questions outlined in the beginning of this articlewere as follows: (a) Would patients with semantic dementiashow impaired episodic memory for verbal material? (b)Would there be a clear impact of the status of semanticknowledge for individual words on episodic learning andmemory for these items? and (c) Would the patients producephonological errors in verbal free recall for unknown words(as previously described by Patterson et al., 1994, for im-mediate serial recall of short sequences of words)?

The experiment revealed deficits on all components of theverbal memory tests in semantic dementia: All 7 patientsshowed poor immediate and delayed free recall of wordlists, even for words on which they had succeeded in priortests of picture naming and word–picture matching (knownwords). In terms of the effects of semantic knowledge, therewas a numerical advantage for known compared with un-known words on all tests, which was statistically reliable onthe third immediate recall trial (but not on the first two trials,probably because performance was so low even for knownwords) and also significant in both the delayed recall anddelayed recognition memory components. The advantagefor known words was especially striking in the recognitionmemory task (see Figures 2 and 4).

Analyses of incorrect responses by the 5 patients whomade errors of commission in free recall revealed that themajority of the errors in the known condition were seman-

tically related to targets. In the unknown condition, bycontrast, the patients were most likely to produce phono-logical errors, including phonological blends in which thepatient produced a word comprising phonemic segmentsfrom within-list items (e.g., “ thistle” instead of thimble andwhistle; and “peal” instead of pipe and seal). In summary,we have obtained positive answers to all three of the ques-tions posed in this study.

Multiple Input Account of New Learning

We have already demonstrated that patients with seman-tic dementia can show preserved new learning as measuredby recognition memory for pictures of familiar objects(Graham et al., 1997, 2000; Simons et al., in press) andfamous faces (Simons et al., 2001), even if they haveimpoverished conceptual knowledge about the stimulusitems. At later stages of the disease, and to some extentdependent on the spread of atrophy to medial temporal loberegions (Simons et al., 2001), recognition memory can beimpaired—although it is notable that even in patients withseverely compromised semantic memory, performance onrecognition memory is rarely at chance (Graham et al.,2000; Simons et al., in press). As we discussed earlier, thisrelative preservation of recognition memory for pictures insemantic dementia is contrary to views of long-term mem-ory in which episodic new learning is entirely dependent onsemantic memory (Tulving, 1995; Tulving & Markowitsch,1998). Instead, we have suggested that the data from se-mantic dementia support a model of human long-term mem-ory in which perceptual information about studied itemsmay be sufficient—in the context of impoverished outputfrom semantic memory—to support successful discrimina-tion between old and new items in an episodic memory test(for more details, see Bruce, 1982; Graham, Patterson, &Hodges, 1999; Graham et al., 2000; Simons et al., 2001).

This multiple input view predicts that a significant impactof semantic status on tests of recognition memory should beobserved for stimulus items that do not provide sufficientperceptual information to support the episodic decision attest. The data from this experiment are consistent with thishypothesis: The patients with semantic dementia showedstrikingly poor recall and recognition memory for wordlists, with a consistent advantage for words that the patientsstill knew according to assessment of semantic knowledgein a pretest. In certain circumstances, therefore, the multipleinput view concurs with the SPI model (Tulving, 1995) inproposing that episodic memory requires input from a func-tioning semantic system.

Why Is Verbal Recall So Impaired, Even for KnownItems?

The patients were extremely impaired on both immediateand delayed recall even for items that were supposedlyknown to them. The stimuli for this experiment were chosenby asking participants to name target pictures and to selectthem, in response to a spoken name, from an array of foursemantically related pictures. An item was only included in


the known word sets if a patient was able to name as well aspoint to that item correctly. Given that the items could benamed correctly by the patients at pretest and that naming isa verbal task that is highly sensitive to semantic breakdown(Lambon Ralph, Graham, Ellis, & Hodges, 1998; LambonRalph, McClelland, Patterson, Galton, & Hodges, 2001), itmight seem surprising that immediate and delayed recallwere poor in the known condition.

A recent study by Lambon Ralph, Graham, Patterson, andHodges (2000), however, illustrates one factor that mayhave contributed to the poor performance on recall: impov-erished activation of semantic memory via words. LambonRalph et al. (2000) investigated the issue of modality effectsin semantic memory by asking patients with semantic de-mentia to define concrete concepts either from presentationof a picture or from its spoken name. The patients werestrikingly impaired in the definitions task, with the majorityof the patients producing more correct information to pic-tures than to words. A similar advantage for pictures overwords has been demonstrated in semantic sorting tasks inpatients with semantic dementia (Rogers et al., 2001). Theexplanation for this discrepancy offered by Lambon Ralphet al. (2000) and Rogers et al. (2001) is that there is a degreeof systematicity in the relationship or mapping betweenpictures and concept meaning but a completely arbitrarymapping between word structure and meaning. Recall thatin the present study, items were classified as known on thebasis of naming and pointing tasks involving pictures,whereas the stimulus input for the episodic memory testsoccurred only in word form. We therefore suggest that evenfor the patients’ so-called known items, the semantic rep-resentations activated by words are impoverished relativeboth to normal control participants and to representationsthat would be activated by pictures in the same patients.This is almost certainly one factor explaining the patients’poor recall for known words.

Another factor that probably contributed to the discrep-ancy between picture naming and verbal list recall is theincreased demands placed on the patients in the memoryexperiment. In picture naming, the patients were presentedwith one picture and asked to produce a single verbal label.In the recall test, they were presented with 10 words andasked to recall as many of these items as possible, bothimmediately and after a delay. As noted earlier, althoughDigit Span is typically within the normal range in semanticdementia, short-term verbal memory as assessed by imme-diate serial recall of unrelated word sequences is oftenimpaired, especially for unknown (previously familiar)words (Knott et al., 1997; Patterson et al., 1994). Thisphenomenon has been attributed in part to the high phono-logical load required for list recall. We have argued abovethat the semantic representations activated by word inputeven for known words are likely to be impoverished insemantic dementia. This factor in interaction with the pho-nological load required to recall a list of 10 words isprobably sufficient to explain the patients’ poor recall ofknown as well as unknown words. More generally, weconclude that although picture naming has been shown to bea sensitive measure of early semantic degradation (Lambon

Ralph et al., 2001), successful retrieval of multiple vocab-ulary items in the absence of pictorial input may be evenmore susceptible to semantic degradation and clearly neces-sitates a fully functional semantic memory system.

Factors That Affect New Learning

New learning in semantic dementia is a topic of theoret-ical and clinical interest because these patients typicallyshow significantly better episodic memory, in the context ofpoor semantic knowledge, than patients with medial tem-poral lobe damage (e.g., patients with Alzheimer’s diseaseand those who have suffered focal lesions to the hippocam-pus and related structures). As we mentioned earlier, se-mantic dementia is typically associated with focal atrophyof the inferolateral temporal neocortex. The status of medialtemporal regions is controversial: Initially it was thoughtthat patients with semantic dementia had relative preserva-tion of the hippocampus and closely related structures(Graham & Hodges, 1997; Harasty, Halliday, Code, &Brooks, 1996). More recent studies have revealed, however,that there is atrophy in parahippocampal regions and to alesser extent in the hippocampus (Chan et al., 2001; Galtonet al., 2001). Given the striking difference in cognitiveprofile between patients with presumed early Alzheimer’sdisease and those with semantic dementia, yet the apparentmedial temporal abnormalities in both patient groups, theissue of new learning in semantic dementia—and the rea-sons for the relative preservation of some aspects ofepisodic memory—becomes of substantial theoreticalimportance.

As demonstrated in the experiment described here, someaspects of episodic memory are compromised in semanticdementia. Many factors (both cognitive and neuroanatomi-cal) therefore need to be considered to understand the cir-cumstances under which one sees preserved or impairednew learning. Investigations that have correlated cognitiveperformance with neuroanatomical measures suggest thatthe status of the parahippocampal gyrus, including theperirhinal cortex, is critical for recognition memory. Simonset al. (2001) documented good recognition memory forfaces in semantic dementia patients with predominantlyleft-temporal lobe damage, whereas cases with the greaterbalance of atrophy in the right-temporal lobe were signifi-cantly impaired on this task. Correlational analyses furtherimplicated the parahippocampal gyrus (which includedsome of the perirhinal and entorhinal gyrus), although de-gree of damage to the hippocampus was also significantlycorrelated with performance. In a similar study, volumetricmeasures of the parahippocampal gyrus bilaterally predictedperformance on a recognition memory test for objects (Si-mons et al., in press). These two experiments demonstratethat structures in the parahippocampal region play a criticalrole in recognition memory for pictures of objects and faces(as predicted by Aggleton & Brown, 1999). Given thesignificant decrement observed in the current study forrecognition as well as recall of word lists, further studiescorrelating verbal memory performance with areas of sig-nificant atrophy may well reveal the importance of medial


temporal regions in the left hemisphere, in particular thehippocampus for measures of recall and the parahippocam-pal region for recognition memory.

Cognitively speaking, modality of input in interactionwith status of semantic memory clearly influences newlearning in semantic dementia. As reviewed above, previousstudies from our laboratory have documented good recog-nition memory for pictures of common objects or famousfaces, even if the patient in question was shown to haveseverely impoverished conceptual knowledge about thoseunknown items, so long as the pictures at study and testwere identical. Only under conditions of perceptual changein the picture of an item from study to test did semanticstatus yield a significant impact on recognition success(Graham et al., 2000; Simons et al., 2001). By contrast,recognition memory for words by the patients in the currentstudy was strikingly impaired and significantly more so fornow unknown words. This is presumably because wordsoffer little perceptual information as a basis for encodinginto episodic memory, forcing reliance largely on wordmeaning.

Effects of Delay: A Cortical ConsolidationExplanation

It has been suggested that patients with semantic demen-tia may show abnormally fast forgetting, in particular forstimuli that are no longer known to the patient (Murre,Graham, & Hodges, 2001). A theoretical account of thispattern is that in healthy people, overwriting of new mem-ories is counteracted by cortical consolidation—the gradualformation of a more permanent memory in the neocortex. Insemantic dementia, there is likely to be poor consolidation,as the brunt of the pathology is found in the neocortex, withthe result that there is nothing to compensate for the over-writing of memories dependent on the medial temporallobe.

To date, there have been few studies of forgetting insemantic dementia. One exception is a case study byGraham, Patterson, Pratt, and Hodges (1999), in whichD. M. showed rapid loss of vocabulary (as measured bycategory fluency) once he stopped daily practice. This de-cline was particularly evident for categories of stimuli thatwere less well known to D. M., suggesting that a delaybetween learning and test might affect memory for un-known more than known stimuli. The results from the studypresented here are consistent with this picture: The patientswith semantic dementia were more impaired on the delayedrecall and recognition component for unknown comparedwith known words. It is important to note, however, thatthere was a significant difference between the two condi-tions by Trial 3; it is thus not clear whether the subsequenteffects of knowledge reflect a differential rate of forgettingor different degrees of episodic learning for known versusunknown items.

Summary

This study documents two important findings in semanticdementia: (a) a direct impact of degraded semantic memory

on episodic new learning for word lists and (b) a significantand pervasive deficit in verbal recall and recognition, evenfor so-called known words. Furthermore, the patients pro-duced phonological errors in free verbal recall of supra-spanword lists, similar to those described previously for imme-diate serial recall of short (three- to four-word) strings offamiliar words with degraded meanings (Graham, Patterson,Pratt, & Hodges, 1999; Knott et al., 1997; Patterson et al.,1994). Although the finding of a significant relationshipbetween semantic memory and episodic recall might betaken as support for a model of long-term memory in whichepisodic memory is always dependent on semantic input (asproposed by Tulving, 1995; Tulving & Markowitsch, 1998),a fuller range of results is explained by a theory in whichepisodic memory receives multiple inputs from perceptualand semantic systems. In circumstances where there is littleor no perceptual information available about studied items,as in memory tests based on vocabulary, semantic knowl-edge about studied items is critical for successful episodicmemory. Where richer perceptual information is providedby stimulus items, however, via pictures of objects or faces,lack of semantic knowledge about targets will not necessar-ily impair performance on recognition memory. The secondfinding, that verbal memory is significantly impaired insemantic dementia, requires further investigation. Even onknown stimuli, patients were severely impaired at immedi-ate recall and even more so after a 10-min delay, whereasthe control participants’ recall revealed no decline after thisshort delay. The most plausible explanation is that verbalstimuli do not produce a normal level of semantic activationin patients with semantic dementia and that impoverishedinput from the semantic system, when combined with thephonologically demanding task of recalling a supra-span listof words, spells trouble for episodic memory.

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Received August 20, 2001Revision received January 24, 2002

Accepted February 26, 2002 �


Multiple inputs to episodic memory: Words tell another story

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