Brain (1998),121,633–646

Category specific semantic loss in dementia ofAlzheimer’s typeFunctional–anatomical correlations from cross-sectionalanalyses

Peter Garrard,1 Karalyn Patterson,2 Peter C. Watson2 and John R. Hodges1,2

1University Neurology Unit, Addenbrooke’s Hospital and Correspondence to: Professor John R. Hodges, MRC2MRC Applied Psychology Unit, Cambridge, UK Applied Psychology Unit, 15 Chaucer Rd, Cambridge

CB2 2QQ, UK

SummaryIn the context of focal brain injury, selective loss of semanticknowledge in the domain of either natural kinds or artefactsis usually considered to reflect the differential importance oftemporal and frontoparietal regions to the representations ofperceptual and functional attributes, respectively. It is harderto account for as a feature of a more diffuse process, andprevious cross-sectional analyses of patients with dementiaof Alzheimer’s type (DAT) have differed over whether categoryeffects occur. In our series of 58 patients with probable DAT,we demonstrated a significant group advantage for artefacts,and explored possible reasons for the inconsistency of thisfinding in other studies. A multiple single-case strategyrevealed not only individuals with consistent advantages for

Keywords: category specificity; dementia of Alzheimer’s type; semantic memory

Abbreviatons: DAT 5 dementia of the Alzheimer’s type; MMSE5 Mini-Mental State Examination

IntroductionIt is now well established that brain-damaged individualsmay show a loss or breakdown of specific categories ofsemantic knowledge (Patterson and Hodges, 1995). The mostfrequently documented dissociation is between the broadclasses of natural kinds and artefacts. The majority of reportedcases have shown a selective loss of knowledge in the domainof natural kinds (Warrington and Shallice, 1984; Hartet al.,1985; Bassoet al., 1988; McCarthy and Warrington, 1988;Pietrini et al., 1988; Sartori and Job, 1988; Silveri andGainotti, 1988; Farahet al., 1989; Hillis and Caramazza,1991; Silveri et al., 1991; Hart and Gordon, 1992; Sartoriet al., 1993; Sheridan and Humphreys, 1993) but the factthat the reverse dissociation has also been reported(Warrington and McCarthy, 1983, 1987; Sacchett and

© Oxford University Press 1998

artefacts but also individuals with consistent advantagesfor natural kinds. By ranking the individuals according tomeasures of naming performance and global intellectualability, we showed that the strength of the group advantagefor artefacts was dependent on the former but not the lattervariable. The findings are discussed in the context of twocompeting theories of semantic breakdown in DAT. Onedifferentiates between domains of knowledge in terms ofthe structure of semantic representations within a singledistributed network; the other emphasizes the importance ofdifferent brain regions in the category distinction. Weconclude that our findings are in keeping with the predictionsof the latter hypothesis.

Humphreys, 1992) probably rules out an artefactualexplanation (Shallice, 1988). The basis of this finding remainscontroversial, but it is now widely accepted that the living/man-made dichotomy captures a fundamental difference inthe nature of the representations underlying different semanticcategories, rather than simply reflecting the presence of twodistinct knowledge systems; knowledge about one class ofobjects (dominated by natural kinds) is thought to be encodedprincipally in terms of perceptual features (size, shape, colour,etc.), while functional attributes are more salient for anotherclass of objects (dominated by artefacts). Thus, damage tothe neural systems critical for the representation of perceptualattributes will result in disproportionate loss of knowledge ofnatural kinds. This explanation, first advanced by Warrington

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(1982), accounts for some apparently anomalous findings inthe experimental literature, such as the fact that parts ofliving things (i.e. body parts) tend to cluster with artefacts,while certain inanimate subgroups (fabrics, precious stonesand musical instruments) segregate with natural kinds. Ithas also received support from the recent application ofcomputational neural network models of semantic memory(Farah and McClelland, 1991).

The neuroanatomical substrate of this distinction alsoremains a subject of debate. An advantage for artefacts istypically associated with an aetiology of Herpes simplexvirus encephalitis (which predominantly affectstemporolimbic structures) whilst the opposite pattern moreoften follows damage to frontoparietal regions (Gainotti,1990). This combination suggests that the two patterns mightcorrespond to a broad anatomical divide between two streamsof post-striate visual processing, as postulated by Mishkinet al. (1983) on the basis of behavioural experiments inselectively lesioned Rhesus monkeys. According to thisproposal, a ventral pathway, incorporating the anterior-inferiorportion of the temporal lobes, is essential for objectrecognition while a dorsal pathway, involving inferior parietalregions, subserves object localization. More recently, PETactivation studies on cognitively normal volunteers haveadded weight to this idea (Mummeryet al., 1996) bydemonstrating distinct regions of brain activation duringsemantic tasks based on categories from each domain. Adifferent, but related dissociation has been documented byGoodaleet al. (1991): a patient with limited occipital corticaldamage secondary to carbon monoxide intoxication wasunable to make visual judgements about line orientationbut could perform highly accurate visually guided handmovements in response to the same stimuli. The richness ofcorticocortical interconnections in the inferior parietal lobeshas led to the hypothesis that this region serves a supramodalsensory function by which visuospatial, tactile andkinaesthetic information is integrated, and would thereforebe a likely substrate for the representation of functionalknowledge. More directly perceptual features, such as colourand shape, are believed to be separately represented in thetemporal lobes (Warrington and McCarthy, 1987). It is thusa plausible extrapolation from both neuropsychological andanatomical data that different aspects of object knowledge,supported by separate brain regions, underlie the categoricalfractionation of semantic knowledge.

Although some degree of semantic impairment iscommonly seen in the early stages of dementia of theAlzheimer’s type (DAT) (Bayles and Tomoeda, 1983; Martinand Fedio, 1983; Chertkow and Bub, 1990; Hodgeset al.,1990; Nebes and Brady, 1990; Hodgeset al., 1991; Hodgesand Patterson, 1995; Patterson and Hodges, 1995; Gonnermanet al., 1997) it is not yet clear whether this deficit ischaracterized by category specificity. Some cross-sectionalstudies have demonstrated no overall category specificity(Hodgeset al., 1992b; Gonnermanet al., 1997); others havedocumented a degree of selective loss of knowledge of

natural kinds (Silveriet al., 1991; Montaneset al., 1995)and ascribed this to the predilection of pathological changesfor temporal lobe structures in the early stages of DAT.Gonnermanet al. (1997) found no significant categoryspecificity in a group of DAT patients as a whole, but theapplication of a multiple single-case approach identified notonly individuals with consistent advantages for artefacts butalso individuals with consistent advantages for natural kinds.This finding sits uneasily with the notion that the disturbanceof semantic knowledge in early DAT reflects a predominanceof temporal lobe pathology, and points instead either to agreater heterogeneity in the spectrum of pathological loci inearly DAT, or to a revision of our notion of how categoriesof knowledge may be selectively disrupted.

Gonnermanet al. (1997) rejected the explanation basedon the spread of pathology to different specialized anatomicalregions and proposed instead that the cognitive structure ofrepresentations in the semantic network will make certaincategories of knowledge more vulnerable to the initial ravagesof a diffuse neurodegenerative disorder. This hypothesisassumes that the semantic impairment in DAT is caused bya diffuse disease process affecting many parts of a distributednetwork of semantic representations simultaneously and that,by virtue of a difference in their structures, representationsof natural kinds and artefacts should disintegrate at differentrates. Gonnermanet al. (1997) based their proposal on thefollowing specific premises. (i) Most concept representationscontain groups of features that characteristically occurtogether; these features may therefore be regarded as being‘intercorrelated’ (Keil, 1987, 1989). (ii) Perceptual featuresof objects intercorrelate to a greater degree than functionalfeatures. (iii) Mental representations of natural kinds aredominated by perceptual features, while functional featurescontribute more heavily to the representations of artefacts.(iv) Similarly, the distinguishing features unique to a concept(i.e. those which allow it to be differentiated from otherexemplars of the same category) tend to be functional featuresin the case of artefacts and perceptual features in the case ofnatural kinds.

Gonnermanet al. (1997) argued that the larger numberof intercorrelated attributes contributing to the conceptualrepresentation of natural kinds will make these less vulnerablein the early stages of DAT. On the other hand, with moresevere deterioration of features associated with advanceddisease, the collapse of this correlational structure shouldyield exaggerated deficits for natural kinds. By contrast,according to this hypothesis, semantic representations ofartefacts will be equally vulnerable at all stages of the disease,and so deteriorate in a linear fashion. The resulting profileof any given DAT patient over time should, therefore, showan early tendency towards a natural kinds advantage, followedat a later stage by a catastrophic loss of natural kind categoriesand hence a reversal of the pattern to an advantage forartefacts. A stylized representation of this putative profile isshown in Fig. 1.

Clearly, variations in the rate of accumulation of

Category specificity in DAT 635

Fig. 1 Profile of longitudinal changes in semantic knowledge forartefacts and natural kinds according to the model of Gonnermanet al. (1997). (Reproduced with permission of the authors.)

pathological changes in DAT as well as in the precisestructure of each individual’s knowledge representations willrender the time course of this process unpredictable, andvariations in the duration of disease before diagnosis willresult in the profiles of individual patients beginning atdifferent points along the curve. However, three testablepredictions about individual profiles do follow from thismodel. The first is that, in any cross-sectional analysis of areasonably large-sized group of DAT patients, there will besome individuals who show advantages for one category andothers with advantages for the other category. The second isthat, on measures of disease severity, patients showing asignificant advantage for artefacts will be at a more advancedstage of disease progression than those showing a naturalkinds advantage. The third is that, for patients studiedlongitudinally, a change from a natural kinds to an artefactsadvantage may be seen, but not the reverse.

By contrast, a more neuroanatomical account of categoryspecificity in DAT is based on the observation that the earliestcortical changes selectively involve the transentorhinal zoneof the temporal lobes (Braak and Braak, 1991), thereafterthe changes evolve to incorporate the temporal neocortexproper and, typically, only spread to inferior parietal regionsstill later in the disease. The notion that the temporal regionis especially important in the representation of perceptualattributes yields the prediction that the earliest and mostpredominant pattern will be one of disproportionate loss ofknowledge about natural kinds. However, the existence ofatypical cases in which other areas of association cortex,including frontoparietal regions, are affected early in thedisease (Rosset al., 1996) does allow for the appearance ofoccasional patients with an advantage for biological kinds.

The accumulated data on semantic performance from ourlarge series of DAT patients has allowed us to test some ofthe predictions made by these two hypotheses.

MethodsSubject groupData from two groups were used for this study: (i) 58 patientswith a diagnosis of probable DAT [31 females and 27 males,

mean age 68 years (SD 8.8), mean years of education 11.6(SD 3.3), mean Mini-Mental State Examination (MMSE)score 19.9 (SD 7.3)], and (ii) 46 normal control subjects [34females and 12 males, mean age 72.9 years (SD 9), meanyears of education 10.42 (SD 2), mean MMSE score 28.9(SD 1.3)]. Written informed consent had been obtained fromall subjects, or the caregivers where appropriate. The studywas approved by the Ethics Committee of The Addenbrooke’sHospital, Cambridge.

The DAT group was drawn from an unselected consecutiveseries of 60 patients who presented to a Memory DisorderClinic at Addenbrooke’s Hospital in 1991–2, and who werewilling to be enrolled into a longitudinal study of semanticmemory and related cognitive deficits in DAT. The diagnosisof probable DAT was made according to the criteria developedby the National Institute of Neurological and CommunicativeDisorders and Stroke and the Alzheimer’s Disease andRelated Disorders Association, which consist of inclusionand exclusion criteria (McKhannet al., 1984). All patientspresented with progressive cognitive impairment,predominantly affecting memory, with a history of between1 and 4 years. In all cases there has been a decline inperformance affecting two or more areas of cognition, asassessed by a wide range of neuropsychological measures.As well as those described in detail below, these includedthe following standard clinical tests: the MMSE (Folsteinet al., 1975); the Dementia Rating Scale (Mattis, 1992);Judgement of Line Orientation (Bentonet al., 1983); ComplexFigure Test (Lezak, 1983); object matching (unusual views)(Humphreys and Riddoch, 1984); and digit span.

Patients with a past history of known or suspected transientcerebral ischaemic event or stroke, alcoholism, head injuryor major medical illnesses (e.g. cancer or thyroid dysfunction)were excluded, as were those with major depression. Allpatients were examined by a senior neurologist (J.R.H.) andby a senior psychiatrist (Dr G. Berrios) at entry to thestudy. In addition to a clinical assessment, all patients wereadministered a number of standard psychiatric rating scales,including the Beck Depression Inventory (Becket al., 1961),to exclude significant psychiatric disorders. All underwentCT or MRI scanning together with the usual battery ofscreening blood tests to exclude treatable causes of dementia.Also excluded were patients with either semantic dementiaor primary progressive non-fluent aphasia as defined inprevious studies by our group (Hodgeset al., 1992a; Hodgesand Patterson, 1996).

Normal control subjects were members of the MRCApplied Psychology Unit subject panel, matched with theDAT patients on the basis of age and education level. Subjectswith a history of alcoholism, drug abuse, learning disability,neurological or psychiatric illness were excluded, as weresubjects with clinically apparent hearing and/or visualhandicaps liable to affect their performance.

Semantic memory test batteryThis battery of tests, all employing one consistent set ofstimulus items, and designed to assess input to and output

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from central representational knowledge about the samegroup of items via different sensory modalities, has beendescribed in detail elsewhere (Hodgeset al., 1992b). Itcontains 48 items chosen to represent three categories ofnatural kinds (12 land animals, six sea creatures and sixbirds) and three categories of artefacts (12 household items,six vehicles and six musical instruments) matched forcategory prototypicality and word frequency. The order ofitem administration is randomized across tests but isconsistent across subjects. The items were chosen from thecorpus of line drawings by Snodgrass and Vanderwart (1980).The following tests were used for the present analysis. (i)‘Category fluency’ for each of the six categories, with 1 minallowed per category. (ii) ‘Naming’ of all 48 line drawingswithout cueing. (iii) ‘Naming in response to verbaldescription’ (e.g. ‘what do we call the small green animalthat leaps around ponds?’, or ‘what do we call a small vehiclewith runners used on snow or ice?’) for 24 of the 48 items(four from each of the six categories). (iv) ‘Word–picturematching’ in response to a spoken word using within-categoryarrays for all 48 items. Subjects are presented with picturearrays consisting of eight items from the same category (e.g.land animals) and asked to point to the item named by theexaminer (the original battery used arrays of six pictures, butin the subsequent version we now use arrays of eight, eachcontaining two foils not otherwise included in the test battery).The subject thus views 48 arrays; these consist of only eightdifferent combinations of items (one for each category suchas land animals), but for each array the position of the targetand foil items is varied. The test sequence is consistent acrosssubjects and is arranged so that each item is followed by onefrom a different category.

Because of the anomalous findings that have been reportedwhen considering the category of musical instruments withinthe domain of artefacts, scores relating to this group ofstimulus items were excluded from the present analysis. Thecategory of water creatures was excluded from the naturalkinds set to preserve the numerical balance. Maximum scoresfor the above tests are therefore 36 for picture naming andword–picture matching (18 per domain), and 16 for namingto description (eight per domain). Category fluency data wereavailable for the four remaining categories (household items,vehicles, land animals and birds).

Analysis 1: overall category specific effectsMethodTo determine whether the patient population exhibited anyoverall advantage in the direction of either natural kinds orartefacts, the probability of correct identification of each itemin the semantic battery at the initial evaluation was calculatedfor picture naming, naming to description, and word–picturematching. All these tests are assumed to require semanticknowledge, and all contain equal subsets of natural kind andartefact stimuli. Category fluency was examined separately,as there is no defined maximum score.

ResultsTable 1 presents the mean probabilities of correctidentification of natural kind and artefact stimuli by patientsand control subjects on each of the three stimulus-basedsemantic tests. After arcsine transformation of the data[recommended by Howell (1992, p. 315) for data of thiskind], a repeated measures ANOVA with two within-itemfactors (patients versus control subjects and confrontationnaming versus naming to description versus word–picturematching) and one between-items factor (natural kinds versusartefacts) was used to analyse these results. Because of thepossible importance of concept familiarity to the phenomenonof selective impairment of semantic categories (Funnelland Sheridan, 1992), the familiarity rating (published bySnodgrass and Vanderwart, 1980) of each item was enteredas a covariate. Significant main effects of group [F(1,33) 561.55, P , 0.001] and test [F(2,66) 5 6.04, P , 0.01]emerged, but there was no significant effect of domain (i.e.natural kinds versus artefacts). There were no significantinteractions.Post hoccomparisons of the scores for each teston the natural kind and artefact subsets revealed no significantdifferences in either subject group (Table 1); the slightnumerical artefact advantage in item identification did notdiffer significantly between the two subject groups [F(1,33)53.15,P 5 0.09].

Mean fluency scores are presented separately in Table 2;they show the expected difference between patients andcontrol subjects [t(102)5 8.24,P , 0.001], but no differencebetween the two semantic domains.

CommentThe absence of a domain-specific impairment across thewhole group is in keeping with the results of Gonnermanet al. (1997) and Hodgeset al. (1992b), but it contrasts withthe artefacts advantage reported in DAT by both Silveriet al. (1991) and Montaneset al. (1995). Of the possibleexplanations for this discrepancy, two can be specificallyaddressed using the present data.

(i) The average stage of disease progression of the patientsmay not be precisely equivalent in all the studies.Gonnerman’s (1997) study population had a mean MMSEscore of 19 and Hodges’ a mean MMSE score of 20.7 witha range of 14–26 (both very similar to the mean MMSE of19.9 in the present sample), while that of the Montaneset al.(1995) patients ranged from 17 to 26, with no mean scorequoted. MMSE was not used in the selection of patients forthe Silveriet al. (1991) analysis. It is therefore possible thatthe two pairs of patient populations may have differedsignificantly on this measure.

(ii) The different stimulus sets used in these studies mayhave introduced unwanted and differing biases. Althoughboth Gonnermanet al. (1997) and Silveriet al. (1991)matched their two sets for item prototypicality, and Silverimatched additionally for frequency, Montaneset al. (1995)

Category specificity in DAT 637

Table 1 Comparisons of the mean probabilities of correct identification of items in thenatural kinds and artefacts subsets, on three tests from the semantic battery

Test MeanP(correct)6 SD

Natural kinds Artefacts t Tests

DAT patients (n 5 58)Picture naming 0.756 0.22 0.796 0.15 t34 5 0.60 (n.s.)Naming to description 0.646 0.19 0.716 0.12 t14 5 0.97 (n.s.)Word–picture matching 0.936 0.05 0.946 0.1 t34 5 0.91 (n.s.)

Control subjects (n 5 46)Picture naming 0.936 0.10 0.976 0.05 t34 5 1.60 (n.s.)Naming to description 0.986 0.03 0.956 0.05 t14 5 1.08 (n.s.)Word–picture matching 1.006 0.02 0.996 0.01 t34 5 0.59 (n.s.)

n.s.5 not significant.

Table 2 Comparison of mean fluency scores

Group Mean fluency6 SD

Natural kinds Artefacts t tests (two-tailed)

DAT patients (n 5 58) 20.36 14.3 21.26 14.0 t57 5 –0.94 (n.s.)Control subjects (n 5 46) 39.76 9.7 40.06 11.3 t45 5 –0.18 (n.s.)

n.s.5 not significant.

matched only for visual complexity; none of these studiescontrolled for concept familiarity, which may be an importantdeterminant of differential performance for the two conceptualdomains (Funnell and Sheridan, 1992).

Additional analyses of the present data were performed toexamine these possibilities.

Analysis 2: effect of non-semantic variablesMethodFirst, to examine whether the absence of a category specificeffect in Analysis 1 might have derived from the overalllevel of disease progression in the population, we dividedthe group into two equal halves on the basis of MMSE score(median split). The first group (n 5 29) had a mean MMSEscore of 25.5 (range 23–30), and the second (n 5 29) a meanMMSE score of 14.31 (range 2–22). The above analyseswere repeated using these two subsets of cases.

Secondly, to test the hypothesis that a category effect mayhave been present, but was eliminated by the partialling outof familiarity in our initial analysis, the original analysis wasrepeated with the concept-familiarity ratings omitted fromthe statistical model.

ResultsTable 3 displays the mean probabilities of correctidentification of items in the natural kind and artefact subsetsfor each of the three stimulus-based tests, using data frommild and severe subgroups of patients as defined above. A

two (group) by three (test) by two (domain) ANOVA againrevealed significant main effects of group [F(1,33)5 18.35,P , 0.001] and test [F(2,66)5 40.19,P , 0.001], but therewas no main effect of domain. There was a significantinteraction between test and group [F(2,66) 5 6.05, P ,0.01], but no interactions involving semantic domain.

The omission of the familiarity ratings from the statisticalmodel had very little effect on the contribution of domain toexplaining the variation inP(correct) (r2 5 0.017 withfamiliarity; r2 5 0.014 without familiarity).

CommentThese findings lend no support to the notion that the presenceof a category specific effect is contingent on the overalldisease progression of the population, and in this regard theyrun counter to the theory of Gonnermanet al. (1997) whichpredicts that an advantage for artefacts is likely to be observedonly at more advanced stages of the disease. Nor do ourresults favour an explanation based on inadequate matchingbetween stimulus sets, according to which category effectsresult from the unequal representation of highly familiaritems in the relatively preserved domain of artefacts.

It is also possible that variation in the size of the patientgroups in the various studies is an important factor. Despitethe lack of an overall group effect, the profile of individualpatients reported by Gonnermanet al. (1997) showed someindividuals with an advantage for artefacts, and others withan advantage for natural kinds. If an artefacts advantage wererelatively more frequent but of smaller magnitude than a

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Table 3 Comparisons of the mean probabilities of correct identification of items in thenatural kinds and artefacts subsets, on three tests from the semantic battery, in twosubpopulations of DAT patients selected on the basis of MMSE

Test MeanP(correct)6 SD

Natural kinds Artefacts t Tests

Mild (n 5 29)Picture naming 0.856 0.18 0.886 0.11 t34 5 0.67 (n.s.)Naming to description 0.696 0.19 0.776 0.12 t14 5 0.93 (n.s.)Word–picture matching 0.986 0.04 0.996 0.03 t34 5 1.16 (n.s.)

Severe (n 5 29)Picture naming 0.666 0.25 0.696 0.20 t34 5 0.32 (n.s.)Naming to description 0.616 0.15 0.676 0.10 t14 5 1.01 (n.s.)Word–picture matching 0.876 0.08 0.896 0.09 t34 5 0.56 (n.s.)

n.s.5 not significant.

natural kinds advantage, then a group advantage for artefactswould be expected to be reported in smaller samples, but tobe balanced out over larger populations. We adopted amultiple single case approach in order to look in detail atthe distribution and nature of category specific impairmentsin individual patients.

Analysis 3: patterns of category specificdissociation in individual casesNaming scoresMethodGonnermanet al. (1997) attributed the absence of an overallcategory effect in their series to the presence of two subgroupsof patients, one showing an advantage for artefacts and theother an advantage for natural kinds, effectively cancellingout any overall category effect. As well as predicting thepresence of both types of dissociation, Gonnermanet al.(1997) argued that there should be a principled relationshipbetween type of advantage and stage of disease, with thecases showing an advantage for natural kinds at a relativelyearlier stage of disease progression than those showing anadvantage for artefacts. This prediction was supported in theGonnerman study by the demonstration that cases with anatural kinds advantage clustered at the beginning of a seriesrank ordered on the basis of success on naming natural kinds.On the other hand, the hypothesis was challenged in ourAnalysis 2 by the finding that both the less and the moresevere halves of our sample, as defined by the MMSE score,exhibited a slight numerical (but not statistically reliable)advantage for artefacts. For a further evaluation of this issue,we applied an analysis similar to Gonnerman’s, by rankingcases according to naming performance on natural kinds.

ResultsFigure 2 displays the differences between the percentagenaming scores on the natural kind and artefact subsets(excluding musical instruments and water creatures) of the

entire population of 58 DAT patients, with cases rank orderedby success on naming of natural kinds. The mean6 2 SDfor the control population is also shown (dotted lines).Although the majority (n 5 39) of cases showed no significantadvantage for one category or the other, it is clear thatthere are some individual patients who show advantages forartefacts and others who show advantages for natural kinds.A stringent criterion of significance was applied to thesecases, requiring an excess advantage of at least one item(5.6%) correct over the values at the extremes of the central95% of control data (dotted lines). This condition was metby 11 cases, of which eight showed an advantage for artefactsand three an advantage for biological kinds. Examining thedistribution of these cases, it is apparent that all those witha significant artefacts advantage scored below the median forthe naming of biological kinds (15 out of 18), while two outof the three with a significant biological kinds advantagescored at this level. There thus appears to be a small trendin keeping with the findings of Gonnermanet al. (1997).

This trend was subjected to formal statistical analysis asfollows. The population was divided into two halves, onescoring above and the other at or below the median for thenaming of natural kinds (15 out of 18). For each subject, thedatum of interest was the excess of correctly named naturalkinds or artefacts, but for the sake of consistency withAnalyses 1 and 2 we wanted to continue examining theresponses item-by-item. We therefore looked at the responses(i.e. correct or incorrect) to all possible natural kind–artefactpairs. By this method, the hypothesis of no domain effectcan be formulated using only natural kind–artefact pairs withunequal scores (i.e. either natural kind correct and artefactincorrect, orvice versa) (McNemar, 1955). The statisticaltechnique recommended for a categorical outcome is thehierarchical loglinear model, which is accessibly describedin, for example, Knoke and Burke (1983passim) or Boniface(1995, p. 115). This technique was used to fit ability groupand semantic domain, with item familiarity entered ascovariate. (We argued earlier that familiarity was notimportant in explaining the variation in item identification,

Category specificity in DAT 639

Fig. 2 Differences between naming scores (percentage correct) for biological kinds and artefactsin all 58 DAT patients. Cases are ranked in descending order of success on naming naturalkinds. Reference lines denote control mean6 2 SD.

but our finding did not relate to a specific semantic test.Since there is independent evidence to suggest that conceptfamiliarity may be differentially important in name retrieval,we decided to include it here.)

A significantly greater likelihood of correct identificationof artefacts than natural kinds was found in the low scoringgroup [χ2(1) 5 89.21,P , 0.001], with no difference seenin the high scoring group [χ2(1) 5 0.05, P . 0.8]. Theinteraction between domain and ability group approached,but did not reach, statistical significance [χ2(1) 5 3.48,P 5 0.062].

Since rank ordering according to success at naming livingthings could produce a rather biased picture (specifically, asignificant artefacts advantage is numerically impossible ifthe score on natural kinds is.15 out of 18), we alsoexamined the pattern of category specificity when the caseswere ordered according to each patient’s overall namingperformance. Inspection of Fig. 3 reveals that all but one ofthe cases with a significant category advantage in eitherdirection are in the lower half of the overall namingdistribution (i.e. at or below the median naming score of 30out of 36). This would suggest that category effects are morelikely to become apparent when anomia is relatively severe,but that the direction of such effects is independent of theseverity. Formal statistical analysis by the method describedearlier showed a significant artefacts advantage in both groups[for the high scoring group,χ2(1) 5 7.99,P , 0.01; for thelow scoring group,χ2(1) 5 8.48, P , 0.01], but there wasno significant group by domain interaction [χ2(1) 5 1.51,P . 0.2].

While semantic memory impairment (as assessed by arange of tests including object naming) is a virtually universalfinding in patients with advanced DAT, in patients with mildto moderate disease there is considerable variability inthe degree of semantic memory impairment. We therefore

examined the relationship between category specificity innaming and disease severity based on MMSE (Fig. 4). Thepopulation was divided about the median MMSE score forthe group (MMSE5 23), and the analysis repeated. In thiscase, both high and low MMSE groups again showed asignificant artefacts advantage [for the high MMSE group,χ2(1) 5 6.98,P , 0.01; for the low MMSE group,χ2(1) 531.73, P , 0.001], but the trend towards an interactionbetween group and semantic domain that was observed whenthe cases were ranked by naming of biological kinds did noteven approach significance [χ2(1) 5 0.13,P . 0.7].

Overall performance on tests of semanticknowledgeMethodsIt was observed earlier that a majority of the cases showedno significant advantage for naming in either direction.Although this finding is neutral with respect to the predictionsof Gonnermanet al. (1997), it is conceivable that the stimulusset (36 line drawings for naming) is too restricted to revealall cases in which a category effect is present. Therefore, itis possible that, if a more global estimate of semanticknowledge were used, a larger number of category specificcases might emerge, with a distribution more in keeping withthe predictions of the model of Gonnermanet al. (1997). Acomposite score was therefore derived by summing thepercentage correct scores for naming, word–picture matchingand naming to description, together with fluency scoresexpressed as a percentage of the control mean scores forfluency. The composite score for artefacts was then subtractedfrom the score for natural kinds, and the difference obtained(semantic index) was expressed as a proportion of thecombined scores. Thus a positive index indicates an advantage

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Fig. 3 Differences between naming scores (percentage correct) for biological kinds and artefactsin all 58 DAT patients. Cases are ranked in descending order of success on naming overall.Reference lines denote control mean6 2 SD.

Fig. 4 Differences between naming scores (percentage correct) for biological kinds and artefactsin all 58 DAT patients. Cases are ranked in descending order of MMSE score. Reference linesdenote control mean6 2 SD.

for natural kinds and a negative index an advantage forartefacts.

ResultsFigure 5A displays the semantic index in the 58 patientsranked in order of MMSE score, with the control mean6 2SD indicated on the figure as before. The number of caseswith a semantic index of at least60.1 (n 5 15, 26%), i.e.those showing a significant category advantage, was greaterthan that found in the naming analysis; of these cases, 12showed an advantage for artefacts. Figure 5B demonstratesthe absence of any extreme deviations from baseline in thecontrol group on the same measure. When we took those

cases who had produced some degree of advantage for oneor other of the categories on the naming test (Fig. 4) andassessed their status on composite score (Fig. 5A), noneshifted from an advantage for natural kinds to artefacts orvice versa, and a previous category effect disappeared inonly three cases (Cases 46, 52 and 53 in the rank orderingof Fig. 4). There was thus a broad degree of consistencybetween these two measures. Because of the composite natureof the index it is not possible to perform multiple pairwisecomparisons on these data, but in line with the earlier results,unpairedt tests showed that, irrespective of direction, thedissociations observed in the lower MMSE group were larger[t(56) 5 3.91, P , 0.001] but that the direction was notdependent on the degree of dementia, as determined by

Category specificity in DAT 641

Fig. 5 (A) Semantic index for all 58 DAT patients, with cases ranked in descending order ofMMSE score. Reference lines denote control mean6 2 SD. (B) Semantic index for all 46control subjects. Subjects are arranged in alphabetical order.

MMSE-group membership [χ2(1) 5 1.97, P . 0.1].Furthermore, the three patients with a significant advantagefor natural kinds were all at the more severely impaired endof the MMSE distribution, which is the opposite of thepattern predicted by Gonnermanet al. (1997).

Consistency of the semantic category advantageWe have established that 15 cases showed a significantcategory effect, as judged by a semantic index clearly.2SD either side of the control mean. The question then arises,in respect of these cases: how many of the tests used tocalculate the semantic index showed a dissociation in thesame direction? Does the overall advantage reflect one largedifference in a single test or an accumulation of perhapssmaller but consistent differences? To answer these questionswe selected the six patients with the largest difference inperformance between natural kinds and artefacts and

examined their performance across each of the four subtests.As shown in Figs 6 and 7, in the majority of cases eachpatient performed better (or at least as well) on the samecategory (natural kinds or artefacts) in each of the tasks.

CommentThe above patterns of data suggest that the prevalence ofsome degree of category specificity in a population may beunderestimated if it is based on analysis of namingperformance alone, and this is likely to be a further factorcontributing to its variable appearance in cross-sectionalstudies.

Our findings fit the first prediction of the model ofGonnermanet al. (1997), that any cross-sectional analysis ofa DAT patient series will reveal the presence of semanticcategory advantages in both directions. This is confirmed bythe finding of six individuals within our cohort whose

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Fig. 6 Comparison of scores on individual semantic tests in the three patients with the strongestartefacts advantage (case numbers are based on position in Fig. 5).wpm5 word–picturematching;pn 5 picture naming;nd 5 naming to verbal description;cf 5 category fluency.Closed bars, natural kinds; open bars, artefacts. *Category fluency scores are expressed as apercentage of the control subject mean.

Fig. 7 Comparison of scores on individual semantic tests in the three patients with the strongestnatural kinds advantage (case numbers are based on position in Fig. 5).wpm5 word–picturematching;pn 5 picture naming;nd 5 naming to verbal description;cf 5 category fluency.Closed bars, natural kinds; open bars, artefacts. *Category fluency scores are expressed as apercentage of the control subject mean.

category specific anomia was accompanied, with almostcomplete consistency, by a similar pattern on the remainingsemantic tests (including category fluency in four out of thesix cases).

However, the model of Gonnermanet al. (1997) alsopredicts that those patients showing an artefacts advantagewill be at a more advanced stage of disease progression thanthose showing a natural kinds advantage. This prediction isnot supported by our findings. Using the technique of multiplepairwise comparisons we showed that, as a group, patientswere significantly more successful at naming artefacts, andthat this difference was particularly marked in patients withlow naming scores. Naming ability is, however, a poor indexof general disease severity, and when a more reliable estimate

(MMSE) is used, this difference between high and low abilitygroups is no longer seen. In other words, the rank orderingscreated by these two methods are rather different, and thisresult is also consistent with the finding of other studies, thatthe relationship between disease severity and anomia is non-linear (Bayles and Trosset, 1992; Priceet al., 1993). Somepatients with DAT exhibit marked word-finding problems(consequent upon semantic impairment) early in the courseof the disease, whereas in others this deficit is only a latemanifestation (Hodges and Patterson, 1995). Such a disparitybetween semantic and global impairment in DAT seemsdifficult to reconcile with the idea that the former is theproduct of a diffuse disease process, which is an importantpremise of the model of Gonnermanet al. (1997). By

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contrast, the relative independence of the two deficits can beaccommodated within anatomical models which seek toexplain global impairment on the basis of total disease load,and semantic impairment on the basis of disproportionateinvolvement of infero-lateral temporal lobe structures.Furthermore, the relationship between the size of the artefactsadvantage and the degree of anomia, suggested by Fig. 3, isconsistent in this context with the notion that a predominanceof temporal lobe involvement will produce a disproportionatedegradation of knowledge about natural kinds. The corollaryof this, namely that extensive pathology elsewhere, possiblyinvolving parietal areas, would produce a disproportionateimpairment for artefacts, is not clearly demonstrated by ourdata. It is worth noting, however, that one of the three patientswith a significant deficit in the artefact domain has recentlybeen reported by our group as one of a series of four atypicalDAT patients with a biparietal syndrome at presentation anddisproportionate atrophy and hypoperfusion of both parietallobes on neuroimaging (Rosset al., 1996).

DiscussionOur analyses of the results of tests of semantic knowledgein this large cohort of DAT patients have shown, first, thatwithin such a cohort some individuals display a degree ofcategory specific semantic impairment. In the majority ofthese cases the advantage is for artefacts, but in a smallnumber, an advantage for natural kinds is seen. Thisheterogeneity is reflected in the fact that, across the wholepopulation, the difference fails to achieve statisticalsignificance. The trends in the data can, however, be amplifiedby looking for category differences between all possible pairsof individual stimuli. Using this technique we revealed firstan overall group advantage for artefacts and second asignificant correlation between the degree of anomia and thestrength of this advantage. However, a parallel correlationwith disease stage (as measured by MMSE) was not apparent.We have examined these findings from the point of view oftwo different perspectives on the organization of semanticknowledge in the brain: one which emphasizes the importanceof distinct brain regions in the representation of perceptual andfunctional features and another which additionally postulatesdifferences in cognitive architecture between biological kindsand artefacts concepts. The latter hypothesis has been mostexplicitly expressed by Gonnermanet al. (1997).

The important differences between these two hypothesescan be summarized as follows. (i) Perceptual and functionalattributes in the model of Gonnermanet al. (1997) aredistinguished in terms of their respective internal correlationalstructure, whereas the neuroanatomical account places muchgreater weight on separate brain regions. (ii) For the purposesof the hypothesis of Gonnermanet al. (1997), theaccumulation of pathological changes in DAT must beregarded as a diffusely distributed phenomenon, whilst theneuroanatomical hypothesis requires a systematic spread ofpathological changes to discrete areas. (iii) Gonnermanet al.

(1997) accept an anatomical account of category specificityin Herpes simplex virus encephalitis and MCA territoryinfarction, but reject it for DAT, while we are attempting toprovide a single explanation, applicable to all instances ofthis phenomenon, regardless of aetiology.

We replicated the finding by Gonnermanet al. (1997) ofsome degree of dissociation of semantic categories withinthe patient population. In keeping with their study, we alsofound that our cohort contained a few individual patientswith a significant advantage for natural kinds, and rathermore with the opposite advantage. Although there is someevidence to support the idea that familiarity biases which areinherent in the test materials produce a ‘natural’ advantagefor artefacts, even in the normal population (Funnell andSheridan, 1992), we would none the less argue for thepresence of a genuine neuropsychological effect. Thisconclusion is based upon the consistency of the advantageover a range of measures seen in individual cases, as wellas the fact that the contribution of concept familiarity to theoverall artefact advantage was partialled out in the analysis.

Since a complete assessment of semantic knowledgedepends upon more than naming scores (Garrardet al., 1997),we extended our analysis to incorporate the results of otherrelevant tests. In doing so, we showed not only that thedomain advantages demonstrated in the naming analysis werelargely maintained, but that several previously undetecteddissociated cases also came to light. The resulting, morecomprehensive, analysis still failed to reveal any interactionbetween disease stage and direction of dissociation—one ofthe most important predictions of the model of Gonnermanet al. (1997).

The second major finding was that the degree of categoryspecificity observed in our sample was highly dependentupon the overall level of anomia and presumed semanticimpairment. The generally characteristic trend towards anadvantage for artefacts was significantly enhanced in caseswith more severe anomia. In order to interpret this findingas evidence for diffusely distributed pathological involvementin DAT, it must be assumed that the degree of anomia is areliable measure of overall disease burden, and thereforecorrelated in a linear fashion with other such measures. Ithas been suggested before that there is no such correlation(Bayles and Trosset, 1992; Priceet al., 1993), and thissuggestion is given further support by our finding that thestrength of the artefacts advantage did not vary betweengroups of patients defined as milder or more severe on thebasis of their MMSE scores.

If degree of anomia does not reflect overall disease burden,then we must ask what it does reflect. It is well establishedthat the naming disorder in DAT results, very largely, froma breakdown in the semantic, rather than pre-semantic(visuoperceptual) or post-semantic (speech production) stagesof picture processing (Chertkow and Bub, 1990; Hodgeset al., 1991). Moreover, it has been hypothesized (Hodgesand Patterson, 1995) that the semantic deficit associated withDAT is caused by the spread of disease from its typical

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earliest sites in the transentorhinal region to temporalneocortex proper (Braak and Braak, 1991). However, theclinical variability associated with the early stages of thedisease suggests that occasionally the earliest neocorticalinvolvement may occur in other areas of association cortex,accounting for the biparietal presentation seen in a minorityof cases (Rosset al., 1996). The further assumption thattemporal regions are especially important in the representationof perceptual knowledge, and frontoparietal regions in therepresentation of functional knowledge (Gainottiet al., 1995),extends this prediction: one group should show an advantagefor artefacts and another, smaller subset of patients, theopposite dissociation. These predictions are upheld by theresults reported here, and by those of Gonnermanet al.(1997). Since all these particular individuals are semanticallyimpaired, they would be expected to cluster at the severeend of the spectrum of anomia. Our analysis suggeststhat loss of natural kinds knowledge is disproportionate inAlzheimer’s disease (as proposed by Silveri), but isparticularly pronounced in more anomic individuals. This isaccounted for almost entirely by the clustering of significantdomain effects (mainly showing an advantage for artefacts)at the severe end of the spectrum of anomia, rather than bythe segregation of the few individuals with a natural kindsadvantage at the mild end (see Fig. 3). The latter pattern ispredicted by a distributed hypothesis which assumes thatnatural kinds and artefacts advantages represent early andlate stages, respectively, in the accumulation of disease load.

The distributed model is also open to question onconceptual grounds. Gonnermanet al. (1997, p. 273) explainthe mechanism by which the distinguishing features ofbiological kinds are relatively ‘protected’ from randomlyoccurring damage as arising from the greater density ofintercorrelated features contributing to biological kindsconcepts. It is not clear from their account what makes adistinguishing feature less likely to be a target in the presenceof other intercorrelated features. If it is simply the numberof such features, then the same argument could be madewithout introducing the concept of intercorrelation at all, so‘protection’ must depend crucially upon the fact that suchfeatures are intercorrelated as well as more numerous. In otherwords, intercorrelation must somehow render the features thatparticipate in it preferentially vulnerable, or even somehow‘attractive’, to randomly occurring damage. The model ofGonnermanet al. (1997) fails to specify how this kind ofdifferential vulnerability might be instantiated in neural terms.

In conclusion, the data presented in this study lend nosupport to the hypothesis that category specific semanticimpairment in DAT can be explained solely in terms of thedifferential vulnerability of individual components of a widelydistributed feature network. They do, however, provideevidence compatible with the alternative notion, that categoryspecificity in DAT simply reflects selective involvement ofeither temporal or frontoparietal brain regions. This positionwould clearly be strengthened by corroborative evidencefrom further large scale studies, particularly if they could

incorporate analysis of data from longitudinal patientassessments.

AcknowledgementsThis research was supported by means of a Medical ResearchCouncil project grant to J.R.H. and a Medical ResearchCouncil clinical training fellowship award to P.G.

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Received March 6, 1997. Revised July 23, 1997.Second revision October 10, 1997. Accepted November 17, 1997