semantic category dissociations: a longitudinal study of two cases

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SEMANTIC CATEGORY DISSOCIATIONS: A LONGITUDINAL STUDY OF TWO CASES Marcella Laiacona 1 , Erminio Capitani 2 and Riccardo Barbarotto 2, 3 ( 1 Salvatore Maugeri Foundation, Rehabilitation Institute of Veruno, Italy, IRCCS, Division of Neurology, Service of Neuropsychology; 2 Clinic for Nervous Diseases, Milan University, S. Paolo Hospital; 3 Istituto di Riabilitazione per Disabili Psichici, Villa S. Ambrogio, Fatebenefratelli, Cernusco S/N) ABSTRACT We report the neuropsychological findings of two patients (LF and EA) with herpes simplex encephalitis. Both patients presented a greater deficit for living than non-living categories in a number of tasks, although EA was much more impaired than LF. We controlled the several stimulus variables that might affect the performance and could demonstrate that the dissociation was not artifactual. Neither LF nor EA revealed a selective or preferential involvement of perceptual semantic knowledge, and both showed a homogeneous impairment of perceptual and associative encyclopaedic notions. At a second examination, carried out from 1 to 2 years later, LF showed a good recovery, whereas EA’s improvement was confined to the non-living categories. The lesion of both patients affected the left temporal pole and the basal neocortical regions of the left temporal lobe. The involvement of limbic areas was more marked in LF, while the Wernicke area and the posterior parts of the middle and inferior temporal gyri were only involved in EA. Besides the basal temporal areas, also the posterior temporal regions are likely to play a role in determining the clinical picture of such patients, and their prospect of recovery. INTRODUCTION A growing body of data from people with acquired disorders of semantic memory has added new information to our knowledge about the phenomenon of category specificity. We will consider here the dissociation between ‘living’ and ‘non-living’ categories that has been found in a number of tasks, including naming, verbal comprehension, questionnaires or visual reality judgements. The most frequent type of dissociation is that where living categories are impaired and many case reports have added to the orignal study by Warrington and Shallice (1984). The opposite pattern is definitely less represented in the literature. Cases of typical dissociation are often associated with herpes simplex encephalitis (HSE), temporal lobe degenerative atrophy or trauma. The anatomical substrate of living categories impairment is likely to include inferior and basal regions of the temporal lobes, with a possible participation of the hippocampus and parahippocampal gyri. Some authors (Gainotti, Silveri, Daniele et al., 1995) have hypothesised a different effect of left or right lesions, with a left lesion impairing only verbal tasks, and a bilateral lesion also involving purely visual tasks. Cortex, (1997) 33, 441-461

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SEMANTIC CATEGORY DISSOCIATIONS:A LONGITUDINAL STUDY OF TWO CASES

Marcella Laiacona1, Erminio Capitani 2 and Riccardo Barbarotto2, 3

(1Salvatore Maugeri Foundation, Rehabilitation Institute of Veruno, Italy, IRCCS, Division of Neurology, Service of Neuropsychology; 2Clinic for Nervous Diseases, Milan

University, S. Paolo Hospital; 3Istituto di Riabilitazione per Disabili Psichici, Villa S. Ambrogio, Fatebenefratelli, Cernusco S/N)

ABSTRACT

We report the neuropsychological findings of two patients (LF and EA) with herpessimplex encephalitis. Both patients presented a greater deficit for living than non-livingcategories in a number of tasks, although EA was much more impaired than LF. We controlledthe several stimulus variables that might affect the performance and could demonstrate thatthe dissociation was not artifactual. Neither LF nor EA revealed a selective or preferentialinvolvement of perceptual semantic knowledge, and both showed a homogeneous impairmentof perceptual and associative encyclopaedic notions. At a second examination, carried outfrom 1 to 2 years later, LF showed a good recovery, whereas EA’s improvement was confinedto the non-living categories. The lesion of both patients affected the left temporal pole andthe basal neocortical regions of the left temporal lobe. The involvement of limbic areas wasmore marked in LF, while the Wernicke area and the posterior parts of the middle andinferior temporal gyri were only involved in EA. Besides the basal temporal areas, also theposterior temporal regions are likely to play a role in determining the clinical picture ofsuch patients, and their prospect of recovery.

INTRODUCTION

A growing body of data from people with acquired disorders of semanticmemory has added new information to our knowledge about the phenomenon of category specificity. We will consider here the dissociation between ‘living’and ‘non-living’ categories that has been found in a number of tasks, includingnaming, verbal comprehension, questionnaires or visual reality judgements. Themost frequent type of dissociation is that where living categories are impairedand many case reports have added to the orignal study by Warrington andShallice (1984). The opposite pattern is definitely less represented in theliterature.

Cases of typical dissociation are often associated with herpes simplexencephalitis (HSE), temporal lobe degenerative atrophy or trauma. Theanatomical substrate of living categories impairment is likely to include inferiorand basal regions of the temporal lobes, with a possible participation of thehippocampus and parahippocampal gyri. Some authors (Gainotti, Silveri, Danieleet al., 1995) have hypothesised a different effect of left or right lesions, with a left lesion impairing only verbal tasks, and a bilateral lesion also involvingpurely visual tasks.

Cortex, (1997) 33, 441-461

Among the several explanations put forward to account for the preferentialderangement of living categories, the hypothesis of a material-bound artifact(Funnell and Sheridan, 1992; Stewart, Parkin and Hunkin, 1992) has not beenconfirmed (Sartori, Miozzo and Job, 1993; Laiacona, Barbarotto and Capitani,1993). A different and more interesting explanation (Warrington and McCarthy,1983; Warrington and Shallice, 1984; Warrington and McCarthy, 1987) is that,since the acquisition of knowledge of living categories strictly depends onperceptual or sensory data, living categories are especially sensitive to the lossof this type of information. Support for this hypothesis comes from a number ofcase descriptions. Using verbal questionnaires or word definition tasks, Basso,Capitani and Laiacona (1988), Silveri and Gainotti (1988), Sartori and Job(1988), and De Renzi and Lucchelli (1994) have reported cases whereencyclopaedic and functional information regarding living categories, though notcompletely spared, is less affected than structural information. Sartori and Job(1988) and Silveri and Gainotti (1988) have suggested that the definite cognitivelocus related to the selective impairrnent of living categories is the structuraldescription system. Along the same lines, Farah and McClelland (1991), using a PDP approach, have shown that a loss of perceptual information is sufficientto generate a selective deficit of living categories.

However, this explanation does not apply to all typically dissociated cases.Some of them, when given a semantic memory questionnaire, proved to beequally impaired on functional and perceptual notions about living categories(Laiacona, Barbarotto and Capitani, 1993; Sheridan and Humphreys, 1993).Moreover, Laws, Evans, Hodges et al. (1995) have recently reported patient SE,who, at a late assessment after HSE, manifested a selective loss of functionaland encyclopaedic information for living categories, whereas perceptual notionswere spared. The opposite pattern was shown by the patient described by Hartand Gordon (1992), who manifested a selective loss of knowledge for the visualattributes of animals. On the basis of this double dissociation, it seemsproblematic that all cases of typical category dissociation can be explained by an impairment of a unique cognitive mechanism. Some patients could also beimpaired at multiple stages. Perhaps, this is specially true for HSE patients,whose lesion includes a wide range of anatomical structures (Kapur, Barker,Burrows et al., 1994), besides the basal temporal regions of either hemisphere.

At this stage, many questions are still open. Longitudinal data have beenrecently used by Hodges, Patterson and Tyler (1994) in a semantic dementiapatient to yield a better insight into structural questions regarding the cognitivesystem. We concur that studying the recovery of HSE patients could furnishuseful information. There are few such reported findings. Patient JH (Swales and Johnson, 1992) showed a limited relearning of semantic information, and the authors suggest that this was due to an improved access to spared semanticmemory traces. On retesting their patient LA, Silveri and Gainotti (1988) foundthat the deficit was stable. In the case SE cited above (Laws et al., 1995), thepatient was earlier more impaired with animals, but a satisfactory recovery oftheir naming was reported; however, semantic recovery was poor with animatecategories and information about the functional properties of animals remainedseverely impaired.

442 Marcella Laiacona and Others

We report a quantitative and qualitative longitudinal study of two HSEpaıients who at the first examination presented the typical category dissociation.They belong to a wider series of HSE patients (Barbarotto, Laiacona andCapitani, 1996) and have been chosen because they were the only patients fromthis series that were re-examined after a sufficient interval. One of themmanifested a good overall recovery, while the other showed recovery only fornon-living categories. Our aim is to assess how the cognitive processes andanatomical structures that were impaired at the first examination can account for their different outcome.

MATERIALS AND METHODS

Semantic Memory Examination

Semantic memory was tested with the battery described by Laiacona, Barbarotto,Trivelli et al. (1993), based on 60 items selected from the Snodgrass and Vanderwart set(1980). The battery included the following tests: (a) picture naming, (b) pointing to pictureson verbal command, and (c) a semantic memory questionnaire. These tests used the same60 stimuli, equally divided into six categories, three of living things (animals – fruit –vegetables)and three of non-living things (tools – furniture – vehicles).

(i) Picture Naming

We asked the patients to name the 60 pictures from Snodgrass and Vanderwart’s set(1980), presented individually in a random order. Following the criteria described in Laiaconaet al. (1993), synonyms and other acceptable names given by controls were scored as correctresponses.

(ii) Pointing to Pictures after Verbal Command

Patients were asked to point to the picture named by the examiner. For each stimulus, 5 pictures, namely the target and 4 foils, were arranged vertically on a card. The foils belongedto other categories during the first part of the test and to the same category in the second. In both parts of the tests all 60 stimuli were examined. The stimulus category and the positionof the target in the column varied randomly.

(iii) Semantic Memory Verbal Questionnaire

360 questions, 6 for each item, were presented orally in standardised random order. Firstwe provided the name of the item and then we asked the six questions, always in the sameorder: (1) General Superordinate(for the item “apple”: Is it an object, an animal or a plant?)(2) Same Category Superordinate(for the same item “apple”: Is it a tree, a vegetable or afruit?) (3) Subordinate: perceptual attributes(for the item “bicycle”: Does it have wheels,skates, or a propeller?) (4) Subordinate: comparison of perceptual attributes(for the item“apple”: Is it bigger than a cherry?) (5) Subordinate: associative functional features(for theitem “bicycle”: Does it carry one person, about five persons or about hundred persons?) (6)Subordinate: associative contextual features(for the item “apple”: Does it grow on a tree, on the ground or on a bush?). We asked the patient to select the correct response among three orally presented alternatives.

The 240 subordinate questions were also classified as visual or non-visualby 10 judgesaccording to whether the correct information could be gleaned by looking at the object(Laiacona, Barbarotto and Capitani, 1993). The number of judges (out of 10) who gave apositive answer was considered a measure of the ‘visual impact’ of the information.

Semantic category dissociations in HSE 443

The following variables that might influence performance were examined.

Frequencyof the stimulus word in the Italian lexicon (Bortolini, Tagliavini and Zampolli,1972) after logarithmical transformation.

Prototypicality for the stimulus word for a given category, according to Battig andMontague (1969). This was the number of normal subjects (from a sample of 442) whoincluded each item in a list reporting all the exemplars of each category.

Familiarity of the stimulus according to Snodgrass and Vanderwart (1980). Subjects wereasked to rate on a 5-point scale (1 = very unfamiliar), how usual or unusual the concept of the given item was in their realm of experience.

Two difficulty indicesfor each question (Laiacona et al., 1993). They consisted in (a) the percentage of 60 normal elderly subjects who correctly answered to that question, and (b) the rating of the difficulty of each question on a 5-point scale given by ten judges (1 = verydifficult, 5 = very easy).

For the analysis of the pictures the concomitant variables that were taken into accountwere as follows:

Name agreement– the percentage of times the correct name was given by the Italiancontrol sample (Laiacona et al., 1993).

Image agreement– the value given by control subjects on a 5-point scale (1 = lowagreement), when asked to indicate how closely each picture corresponded to their ownmental image of the item (Snodgrass and Vanderwart, 1980).

Visual complexity– the amount of detail or intricacy of lines in the picture itself, judgedon a 5-point scale (1 = very simple), according to Snodgrass and Vanderwart (1980).

Details of these indices are reported by Laiacona et al. (1993) and by Capitani, Laiaconaand Barbarotto (1993). We set the normality threshold at the level of the lowest scores foundin a sample of 60 normal elderly subjects.

(iv) Fluencywas assessed by requiring the patients to produce as many names as possiblebelonging to each of the semantic categories studied in our battery (animals, tools etc.); timeallowed was one minute for each category.

(v) Reality decision task:To detect possible damage to the strucural description system,the patients were requested to discriminate between pictures representing real and unrealthings. We used three kind of pictures: (i) the same 60 pictures from the Snodgrass andVanderwart set (1980) used in the naming task. (ii) 30 pictorial non-real items derived fromthe Kroll and Potter set (1984): they were closed-line drawings with an object-like appearance,created by combining parts of drawings and regularising the resulting pictures. (iii) 30 non-real pictorial foils made by assembling two parts from two pictures of Snodgrass andVanderwart belonging to the same category: for example a frog-head with a mouse-body. 15 stimuli were assembled from living category pictures, and 15 from non-living categorypictures.

For all these tasks we assumed as normality threshold the worst performance observedwith a sample of 60 healthy subjects.

Statistical Methods

(a) Analysis of Single Performances

On each test (naming, pointing to pictures and the semantic memory questionnaire) 1point was assigned to every correct response. Scores were submitted to logistic regression

444 Marcella Laiacona and Others

analysis (McCullagh and Nelder, 1983), making it possible to study, within a linear model,the effects of the variables that might have influenced performance. The model included bothcategorical variables (as the classification of the items as living or non-living) and continuousvariables (as word frequency). For naming and pointing to pictures the model includedstimulus category, word frequency, familiarity and prototypicality of the stimulus, visualcomplexity, image agreement and name agreement. For the questionnaire, the model includedstimulus category, word frequency, familiarity and prototypicality of the stimulus plus thetype of the question (Superordinate versus Subordinate and, within Subordinate questions,associative versus functional), and the Visual / non-Visual content of the requestedinformation; moreover, the models included also the two difficulty indices for each questionas described above.

Interrelations between the terms of the models were studied as interactions (if all werecategorical) or parallelism (if one was categorical and the other continuous). The categoryeffect was evaluated after partialling out its overlap with the other terms of the model. Theeffect of this adjustment can explain why significance levels can be not strictly proportionalto the raw differences. Moreover, it should be born in mind that logistic regression is moresensitive to differences found in proximity of the extreme values.

The analyses were programmed as a macro-instruction of the programme GLIM, release3.77 (Aitkin, Anderson, Francis et al., 1989) as detailed in Capitani et al. (1993).

b) Analysis of Consistency between Repeated Examinations

The analysis of response consistency is a relevant point in the distinction betweendegraded store and access disorder. Faglioni and Botti (1993) suggest a new methodology,based on a stochastic model of retrieval and storage deficit that can be analysed in terms of a general Markov chain. In the case of two trials, the method makes it possible to estimatetwo parameters, representing (i) the percentage of items that are ‘stored’ (i.e. still within thememory after the brain lesion), and (ii) the probability with which these stored items canbe retrieved at each trial. Using this method it is possible to estimate the variance bound tothese parameters, and thereby evaluate whether they significantly differ from 0 or 1. Thismethod was used to analyse the second performance of EA.

Neuroradiological Study

The MRI images were mapped into the templates reported by Damasio and Damasio(1989) in the Appendix of their book on brain lesion analysis. For the description ofanatomical structures, reference was also made to Nieuwenhuys, Voogt and van Huijzen(1978). Findings with patients LF and EA are reported in Figures 1 and 2, respectively.Under each picture we indicate the template of reference: for instance, l5a means that weare using the first template of the set A.15. Lateral reconstruction of the cortical lesion areshown in Figure 3. In some cases, extent and site of lesion may seem to be not perfectlycorrespondent in coronal and axial sections, because available MRI were sometimes carriedout with different T1 and T2 parameters. Moreover, exact definition of the lesion extentmay be difficult with long-T2 images.

PATIENT 1 (CASE LF)

In August 1989, LF, a 43 year-old male, office worker, with 8 years ofschooling, was admitted to the Asti Hospital suffering from headache and fever.On admission he was confused and disoriented. Three EEGs performed in thesame month revealed diffused abnormality prevailing in the left temporal andfrontal regions, while the EEG repeated three months later was normal. CSFexamination showed lymphocytosis (up to 500/mmc) that decreased during thefollowing months (20/mmc). During the two months of hospitalisation, the rate

Semantic category dissociations in HSE 445

of CSF HSV-specific antibody ranged from 1:10 to 1:80, whereas serum HSV-specific antibodies ranged from 1:10 to 1:200.

About 5 months post onset, in February 1990, the patient was referred to the Neuropsychology Unit of Veruno Hospital for memory and languageproblems. At this time he was well oriented in time and place and completelyautonomous in his everyday life. Neurological examination was normal. On astandard neuropsychological assessment LF obtained pathological scores onverbal learning and non-verbal long-term memory and showed retrogradeamnesia. He also underwent a formal language examination (AAT test, Luzzattiet al., 1994) that showed a mild amnestic aphasia.

On this occasion he underwent a semantic memory assessment that wasrepeated 13 months later (18 months post onset). The findings of the semanticmemory examination will be reported separately.

Neuroradiological Findings

An initial CT-scan showed left temporal damage. The MRI, performed 15days later, showed three areas of abnormal intensity: (i) almost the whole lefttemporal lobe (basal portion, medium and inferior gyrus, hippocampus,parahippocampal gyrus including the anterior two-thirds of the lateral occipito-temporal gyrus), while the posterior part of the superior and middle temporalgyri and the underlying white matter were spared; (ii) part of the infero-medialfrontal lobe (the left rectus and cingular gyrus and a small lesion on the orbitalportion of right frontal lobe); (iii) the right temporo-basal region (the central part of the inferior temporal gyrus, the lateral occipito-temporal and theparahippocampal gyrus).

In April 1990, LF underwent a second MRI that still showed severeinvolvement of the left temporal lobe and a small lesion in the right temporo-basal region (mainly affecting the lateral occipito-temporal gyrus). In the lefttemporal lobe there was severe atrophy of the hippocampus, parahippocampaland lateral occipito-temporal gyri, with a widened temporal horn of the lateralventricle; there was also a signal alteration on the amigdalar nuclei and insula,whereas the posterior halves of the upper and middle left temporal gyri weredefinitely less involved (Figures 1 and 3).

Results

(i) Picture Naming

First Examination:As can be seen from Table I, on picture naming LF scoredbelow the norm in terms of the overall percentage, but showed a dissociation in performance between non-living things, that were just at the cut-off point, and living things, that were definitely impaired. In the regression analysis, theliving/non-living things comparison was significant even after adjustment for the other model variables (Chi-square = 8.270, d.f. = 1, p = .004). Among theother variables of the model, frequency, familiarity and name agreement were

446 Marcella Laiacona and Others

Semantic category dissociations in HSE 447

Fig. 1 – Patient LF: MRI diagram showing three areas of abnormal intensity involving almost thewhole left temporal lobe, part of the frontal lobe and the right temporo-basal region. Right side of thediagram corresponds to the left side of the brain.

15a 15b 15c

15d 15e 15f

17b 17d 17e

17f 17g 17i

significant predictors of the performance: Chi-square values (with d.f. = 1) were,respectively, 4.870 (p = .027), 4.681 (p = .031) and 16.969 (p < .000l).

Second Examination:After 13 months, LF performed within the normalrange both on living and non living items.

(ii) Pointing to Pictures

First Examination:LF performed slightly below the cut-off point for livingthings. The comparison between living / non-living things was significant (Chi-square= 10.080, d.f.= l, p = 0.001). None of the concomitant variables wassignificant.

Second Examination:On this occasion the performance of LF was flawlesson both category groups.

(iii) Verbal Questionnaire

First Examination: LF showed a minimal impairment with questionsregarding living things on which he scored significantly lower than on non-living things. As reported in Table I, the comparisons between Superordinateand Subordinate questions, between perceptual and associative questions andbetween visual and non-visual questions were not significant.

Second Examination:The performance was normal for both living and non-living things, even if a significant discrepancy still emerged from the statisticalanalysis. The significance is due to the special sensitivity of logistic regressionto even small differences near the extremes of the scale. However, thissignificance is negligible here, as both measures were within the normal range.

(iv) Fluency on Semantic Cue

Whereas the performance with non-living categories was normal since thefirst examination, LF was pathological with living categories both in the firstand the second examination. In the second examination he was also pathologicalwith musical instruments (2 within one minute), but not with body parts (8within one minute).

(v) Reality Decision

On both sessions LF successfully discriminated existing from non existingstimuli of either category.

Summary of LF

At the first examination only living categories were impaired when assessedwith verbal tasks. The deficit concerned mainly picture naming. The realitydecision test showed that the structural description system was undamaged.Pooling together the responses given in naming, pointing to pictures and thequestionnaire, LF made errors with 28 stimuli (24 living and 4 non-living). In

448 Marcella Laiacona and Others

10 items (9 living stimuli) the errors affected the questionnaire and at leastanother tasks, which suggests a slight degree of central semantic impairment,possibly combined with a deficit of the output phonological lexicon.

After 13 months, LF performed within the norm in all tasks, with the onlyexception of semantic fluency for living categories.

PATIENT 2 (CASE EA)

In December 1990, EA, a 47 year-old male, camp site keeper, with 8 yearsof schooling, was admitted to Gallarate Hospital, with a few days’ history ofheadache, nausea, fever and dysphasia. Neurological examination revealed slightright hemiparesis. Several EEGs performed in the following month showed slow-wave activity in the left anterior temporal region. CSF examination did not showan increase in white cell count (1/mmc). CSF laboratory data showed HSV andHZV-specific IgG antibody.

Semantic category dissociations in HSE 449

TABLE I

Semantic Memory Assessment: Percentage of Correct Responses (100% = 1.00)

Case LF Case EA

1st 2nd 1st 2ndTask Norm examination examination examination examination

Picture NamingOverall ≥ .76 .70* .90 .08* .23*Living things ≥ .67 .53* .83 .00* .03*Non-living things ≥ .87 .87 .97 .17* .43*Living vs. Non-living p = .004 p = .076 p = ns p = .031

Pointing to picturesOverall ≥ .93 .96 1.00 .72* .83*Living things ≥ .93 .92* 1.00 .58* .68*Non-living things ≥ .92 1.00 1.00 .85* .97Living vs. Non-living p = .001 — p = .002 p < .001

QuestionnaireOverall ≥ .92 .93 .95 .69* .69* [78]Living things ≥ .90 .88* .91 .61* .51* 163]Non-living things ≥ .94 .99 .99 .78* .87* [93]Living vs Non-living p = .0003 p = .0022 p = .039 p <.0001 [<.0001]Superordinate ≥ .96 .92* .98 .75* .73* [81]Associative features ≥ .89 .95 .93 .64* .64* [76]Perceptual attributes ≥ .91 .93 .96 .69* .70* [78]Superord. vs. Subord. p = ns p = ns p = ns p = ns [ns]Associative vs. Perceptual p = ns p = ns p = ns p = ns [ns]Visual vs. Non-visual p = ns p = ns p = ns p = ns [ns]

FluencyLiving things n ≥ 18 n = 15* n = 14* n = 3* n = 3*Non-living things n ≥ 12 n = 19 n = 12 n = 9* n = 12

Reality decisionReal Living ≥ .87 1.00 .93 .80* .87Real Non-living ≥ .83 1.00 .97 1.00 .97Meaningless Living ≥ .80 1.00 .87 1.00 .93Meaningless Non-living ≥ .85 1.00 .93 1.00 1.00

* pathological; [...] = Questionnaire presented with pictures instead of orally pronounced names.

In April, 1991 the patient was referred to the Neuropsychology Unit ofVeruno Hospital on account of his language disturbances. He also complained of severe topographical problems; moreover, several aspects of his everyday lifescemed new to him (for example he did not remember owning a motorcycle or how to ride it). The neurological examination was normal. About 4 monthspost-onset, on a standard neuropsychological assessment EA obtainedpathological scores for naming and for long-term verbal memory tasks; retrogradeamnesia was also present. He underwent a formal language examination thatshowed Wernicke aphasia with lexical and semantic errors.

On this occasion and 20 months later (24 months post onset) EA underwenta second semantic memory assessment, followed by a close retest. Findings ofsemantic memory assessment will be presented in a separate section.

Neuroradiological findings

CT-scans performed in Gallarate Hospital showed hypodense areas in the left temporal lobe. An MRI performed 1 year post onset (Figures 2 and 3)confirmed a severe left temporal lobe lesion, which involved the whole anteriorhalf of the lobe (showing widespread necrosis and cystic formations), and moreposteriorly the medium and inferior temporal gyri, the medial and lateraloccipito-temporal gyri and, less severely, the parahippocampal gyrus. Behind the areas affected by cystic necrosis, there was a smaller region that presentedan altered MRI signal, especially in long-T2 sequences, probably caused bygliosis. This region included the Wernicke area and the deep white matter of the posterior temporal lobe. A smaller region of abnormal intensity was alsoobserved in the left hippocampus. The temporal horn of the left lateral ventriclewas enlarged. The left insular region was also damaged. On the right, a smallarea of abnormal intensity was observed in the anterior part of the lateraloccipito-temporal gyrus.

Results

(i) Picture Naming

First Examination:As can be seen from Table I, EA scored very poorly on both living and non-living items, without a significant category difference.

Among the concomitant variables frequency, familiarity and prototypicallywere significant predictors; corresponding Chi-square values (d.f. = 1) were: 9.938(p = .002), 9.161 (p = .002) and 8.500 (p = .004).

Second Examination:After 20 months, picture naming showed someimprovement, restricted to non-living things. Categorical dissociation was nowapparent (Chi-square = 4.640, d.f. = 1, p = 0.031). Frequency and familiarity werestill significant predictors: Chi-squares were, respectively, 17.199 and 15.122,with d.f. = 1 and p < .0001.

To assess what variables influenced the improvement from the 1st to the 2nd examination, we focused on the 55 pictures that EA failed to name in thefirst examination, and carried out a logistic regression analysis in order to see

450 Marcella Laiacona and Others

Semantic category dissociations in HSE 451

Fig. 2 – Patient EA: MRI diagram showing the damaged structures. Right side of the diagramcorresponds to the left side of the brain. On the lefit side, some temporal lesioned areas (shown insections 15a, 15b, 15c, 17d, 17e) were almost destroyed and presented with wide cystic cavities.

15a 15b 15c

15d 15e

17d 17e 17f

17g 17h 17i

whether frequency, familiarity or the stimulus category predicted their naming at the second examination. The effect of each predictor variable was evaluatedafter prorating its overlapping with the other effects, i.e. independently of them.We found that picture naming improved on the basis of the frequency of thecorresponding name (Chi-square= 4.698, d.f.= 1, p= .03) and of its semanticcategory (Chi-square= 5.431, d.f.= 1, p= .02), but not of its familiarity (Chi-square< 1, ns).

On this occasion we analysed the consistency between pictures correctlynamed in two successive presentations with the two-parameter model of Faglioniand Botti (1993). The performance with living things was so poor that noconsistency analysis could be attempted: correct responses were 0 in the test and 1 in the retest. Within non-living items stored names were found to be 54%,with a retrieval probability of 55.5%. The confidence limits of both parametersincluded neither 0 nor 1, and this suggests that both stages (storage and retrieval)were partly damaged.

(ii) Pointing to Pictures

First Examination:The impairment involved both category groups, but wassignificantly more marked for living things (Chi-square= 9.860, d.f.= 1, p = .002). The only significant predictor was visual complexity (Chi-square= 5.970, p= .015), and this variable equally affected living and non-livingitems.

Second Examination:After 20 months the performance with non-living thingsshowed a full recovery (97% correct), even when alternatives belonged to thesame category. On the contrary, living stimuli were still impaired, showing anerror rate of 32%, that rose to 57% with foils of the same category. Thedissociation was significant (Chi-square= 15.321, d.f.= 1, p< .0001).

(iii) Verbal Questionnaire

First Examination:The questionnaire showed impairment on both categories,but the category effect was significant (Chi-square= 4.270, d.f.= 1, p= .039).Superordinate, perceptual and associative questions showed approximately thesame impairment (respectively 60%, 63% and 58% correct in the case of livingthings). Contrasting the questions on the basis of their visual saliency, nosignificant effect was disclosed: for non-living categories the percentage correctwas 84% for non-visual and 73% for visual questions; with living categoriespercentages were 61% in both cases. Frequency and familiarity of the stimulusword were both significant predictors of the success rate, and showed the sameeffect with both categories.

Second Examination:The overall correct rate did not change (69% correct).With living things there was a 10% decline, which contrasted with acorresponding improvement in questions tapping non-living things. As aconsequence, the dissociation became even more significant (Chi-square= 28.905,d.f. = 1, p< .0001). Although these variations may be in part random oscillations,the improvement with non-living things is in line with the trend in naming and

452 Marcella Laiacona and Others

pointing to pictures. The impairment with different types of questions(superordinate, associative and perceptual subordinate; visual and non-visual)was still homogeneous. Frequency, familiarity and prototypicallity significantlyinfluenced the performance.

Consistency analysis was possible only for non-living things, because therewere no living items that were answered correctly on both repetitions.Nevertheless, it can be presumed that the percentage of stored items was low,indicating a severe loss. With non-living things, the percentage of stored itemswas .63 (confidence limits from .41 to .84), whereas retrieval probability was .69 (confidence limits from .49 to .89). A mixed deficit appears to characterisenon-living items. In analogy with the conclusions drawn from the namingconsistency, we can assume that at least some units were not lost, but presentedaccess problems.

Notably, EA never inquired about the meaning of the presented words, nordid he react as if they were unknown to him. In a lexical decision task, whereall the stimulus words were mixed with non-words, he accepted all the existingwords and rejected the non-words.

Visual Presentation of the Stimuli:A few days after the second oraladministration of the questionnaire, we repeated the test presenting the Snodgrasspictures corresponding to the stimulus words, and asking exactly the samequestions. The results, shown in Table I (in square brackets), indicate a moderateimprovement. Performance with non-living things approached the norm. The mostinteresting point is, however, whether picture presentation fostered the retrievalof visual informations in comparison to oral presentation (see Table II).

On living items, EA did not show a clear advantage for visual questions. Athree-factor logistic regression analysis of the data of Table II indicates that only the stimulus category and the type of presentation significantly influencedthe performance, with Chi-squares, respectively, of 60.435 and 4.640 (d.f.= 1, p < .0001, and .03). The third factor (visual vs. non-visual quality of the requestedinformation) was not significant, nor were the first or second order interactionsbetween the main factors. Examples of EA’s errors are reported in Table III.

Consistency analysis between the verbal and visual presentations of thequestionnaire was attempted by classifying the stimuli into two categoriesaccording to whether or not all the 6 related questions were given flawlessresponses. For the 30 living stimuli, we registered 27 double failures, and just 3 cases where the response was inconsistent across presentation (only one of

Semantic category dissociations in HSE 453

TABLE II

Percentage of EA’s Correct Answers to the Questionnaire according to the Semantic Category, theVisual/Non-visual Nature of the Investigated Information, and the Type of Presentation of the Stimulus

(Verbal or Pictorial)

Visual questions Non-visual questions

Non-living things Verbal stimulus .84 .88Pictorial stimulus .95 .92

Living things Verbal stimulus .52 .52Pictorial stimulus .59 .64

them was right with the pictorial presentation). This distribution did not allowfurther analysis. In the case of non-living items, 21 stimuli showed a consistentoutcome (11 right and 10 wrong) and 9 were inconsistent (8 being right with the visual stimulus only). On this basis, and from the analysis of Table II, it can be inferred that visual access to the semantic system through a non-verbalchannel resulted in a general, moderate improvement, but did not solve the bulkof the problems EA presented with living stimuli, which probably came from a deeper semantic deficit. With non-living items the visual questionnaire closelyapproached a normal level of performance, corroborating the hypothesis that thedeficit observed with verbal stimuli was partly due to a defective verbal accessto the semantic system.

(iv) Fluency on Semantic Cue

In the first session (Table I), EA produced just three names of living things(lemon, horse and dog) and 9 of non-living things: both values are pathological.He could produce the names of three body parts and two musical instruments. Inthe second examination names of living things were still three (horse, dog and cat), whereas names of non-living entities had risen to the borderlineperformance of 12; in the same session he was able to produce twelve names of body parts and two names of musical instruments.

(v) Reality Decision

As shown in Table I, at the first examination EA rejected six pictures of real living items (celery, onion, asparagus, salad, pineapple and strawberry). Inthe second examination the rejected real pictures were four living items(asparagus, salad, grapes and caterpillar) and one non-living item (sledge). In a control sample of 60 subjects with low education, who were given the sametask, salad was rejected by 55% of them, caterpillar, strawberry and celery by8%, asparagus by 6.7%, pineapple by 5%, grapes and onion by 1.7%, and sledgeby 14%. EA’s performance with real living pictures was slightly below norm in the first examination and just normal in the second. Findings with non-realpictures and with non-living things were fully within the norm.

454 Marcella Laiacona and Others

TABLE III

Examples of EA’s Errors on Questions Tapping Visual Information after Pictorial Presentation of the Stimulus

Stimulus Question Answer

Giraffe Does it have stiped, uniform or patched hair? Striped hairCamel Does it have a flat back, a humped back or coarse scales? Coarse scalesStrawberry Does it have a peel, a shell or neither? A shellAsparagus Is it rounded, flat or oblong? FlatSalad Does it have leaves, a shell or thorns? Thorns

Summary of EA

In the first examination EA manifested a total loss of living picture naming,but also a poor performance with non-living items. A deficit was also apparent,though on a reduced scale, in pointing to pictures: in this task a 20% correctscore is expected by chance, and a category effect was detected. The same patternwas obtained with the questionnaire, where both categories were defective, butquestions regarding living items were significantly more impaired.Notwithstanding a trend towards a better performance with superordinatequestions, the impairment was homogeneous, and did not reflect any differencebetween perceptual and associative information or of questions tapping visualand non-visual knowledge. Verbal fluency task showed a similar pattern. Thereality decision task pointed to a defective structural description system which,however, cannot be held entirely responsible of EA’s impairment since his deficiton the object decision task was mild, and also associative, non-visual knowledgeproved defective in the questionnaire (see Table II).

On the basis of the impressive impairment in naming, the effect of frequencyand familiarity, and the consistency analysis, we hypothesise that EA wasaffected by a central semantic defect, more severe for living categories, combinedwith a general lexical impairment that affected all categories.

Semantic category dissociations in HSE 455

Fig. 3 – Mesial and lateral views of the left hemisphere drawings.

Patient LF:

Patient EA:

In the second examination EA improved in all non-living categories tasks:naming was still severely impaired and also the questionnaire remained defective,but pointing to pictures showed a full recovery. With living categories EA didnot improve, the only exceptions being pointing to pictures and the realitydecision (Figure 4). In the latter task, EA performed within the normal range,and this confirms that a defective structural description system was notresponsible for his cognitive deficit.

As already remarked, visual presentation of the questionnaire improved EA’sperformance, but living things remained markedly defective.

456 Marcella Laiacona and Others

Fig. 4 – Diagram of patients’ evolution. Due to the low severity of patient LF with non-living,things, in this case the scale goes from 80 to 100, and not from 0 to 100.♦ = naming ● pointing to pictures ■ object decision ▲ questionnaire

Patient LF: living things Patient LF: non-living things

Patient EA: living things Patient EA: non-living things

100

98

96

94

92

90

88

86

84

82

80

DISCUSSION

The impairment presented by LF and EA was restricted to, or more severefor, living categories. In some aspects, their cognitive impairment was similar;for instance neither of them was affected by a prevailing deficit of perceptualinformation. However, our patients were different with respect to generalseverity, to recovery rate and to the brain lesion topography, even if both wereaffected, by and large, by prevailing left temporal lobe lesions. The discussionwill be partitioned according to the relevant questions emerging from the currentdebate on this topic.

True Dissociation or Artifact?

Given that the reality of category dissociation is now ascertained beyondargument, it suffices to say that in the present study all the effects were stillsignificant after covariance for a number of potentially confounding variables,and cannot be considered artifactual. Notably, we also introduced among theconcomitant variables two difficulty coefficients for each question obtained froman inquiry in normal subjects (Laiacona, Barbarotto and Capitani, 1993; Capitani,Laiacona and Barbarotto, 1995), as questions regarding living categories may be basically more difficult than questions regarding non-living categories. Thecategory effect still held true after covariance for these indices.

A Loss Confined to Visual or Perceptual Knowledge?

This is an intriguing question, as some authors have posited that thedistinction within living items is based on perceptual information, whereas non-living items would differ also for their function. Some studies have made anexplicit comparison between the different types of information, i.e. visual vs.perceptual knowledge.

Sartori and Job (1988) analysed a word definition task in their patientMichelangelo and found that perceptual attributes were more frequently correctfor objects than for living categories. However, encyclopaedic attributes of livingcategories were not spared, being wrong in 15 cases out of 46 (33%), against a 45% error rate for perceptual attributes. Their conclusion that ‘the patient hasspecific problems in retrieving correct perceptual attributes for the categories ofanimals and vegetables’ seems not fully warranted. Patient LA (Silveri andGainotti, 1988) was better at identifying animals from functional descriptionthan from visual description, and also these authors concluded that her deficit‘selectively involved her pictorial semantic system’. However, LA still had anerror rate of 42% in her ability to name animals from functional descriptions,like ‘an industrious insect producing honey’. This error rate, though lower thanthat found with animals on visual description (91%), was higher than thatgenerally found with inanimate objects (about 20%). Also in this case, a selectiveloss of pictorial information for animals does not appear to be an exhaustiveexplanation. However, in two other cases non-visual knowledge of living

Semantic category dissociations in HSE 457

categories seems more reliably, though not completely, spared. Giulietta (Sartori,Miozzo and Job, 1993) on her word definitions made just two non-perceptualerrors with animals (‘an elephant is typical of Christmas day’ and ‘a leopardlives in our region’) and was 93% correct in semantic judgements aboutencyclopaedic properties of the same category. Felicia (De Renzi and Lucchelli,1994) was between 73% and 96% correct when asked about encyclopaedicproperties of animals.

At variance with the cases above, patient SB (Sheridan and Humphreys, 1993)showed equivalent levels of visual and non-visual (verbal) information for theanimal category (14/20 and 13/20, respectively). Interestingly, SB did not showsparing of superordinate information either, and this is a further analogy withour cases. Also for the patients described in this paper, the residual associativeinformation regarding living categories was balanced with residual perceptualinformation. In the statistical analysis no significant differences were detected.Neither did LF or EA answer the ‘visual’ questions better than ‘non-visual’ ones and, more interestingly, the analysis of the percentage of correct responsesnever showed an interaction between the effects of ‘visual’ type and category. In other words, the difference between visual and non-visual questions wassimilar for living and non-living categories. In our patients, the failure to detecta disproportionate deficit of perceptual knowledge cannot be viewed as a resultof a low power of the inquiry, as in fact we did detect a deficit of this kind of knowledge, but also found a concomitant deficit of associative andencyclopaedic notions. A reasonable conclusion could be that the selectiveimpairment of living categories is not a homogeneous entity, and tht itsmanifestation does not necessarily depend on the selective loss of perceptualknowledge.

A separate point is why EA did not draw substantial advantage from thevisual presentation of ‘visual’ questions (see Tables I, II and III), for which acontrol group had judged that the answer could be given by simple inspectionof the stimuli. We are here not simply faced with some ‘loss of stored visualinformation’ where the deficit could improve if the missing data are providedalong the visual channel. It might be surmised that EA could not understand the words forming the questions, and (Table III) that he responded that‘asparagus is flat’ because he ignored the meaning of ‘flat’ and not only that of ‘asparagus’.

This is likely to be true, at least for some questions, but in this particularcase the terms ‘rounded, flat and oblong’ are not solely confined to livingcategories; indeed they are words of general use in the description of forms,even of the forms of objects. If this explanation was correct, we would expectalso some deficit with other visual questions regarding objects, but with thelatter category and visual presentation, EA was 95% correct. Moreover, EAnever inquired about the meaning of words appearing in the questions given tohim, nor was he surprised or perplexed during the test. On the whole, thebehaviour of EA remains largely unexplained, and the description of visuallypresented material seems a point worthwhile exploring in future studies of HSEpatients.

458 Marcella Laiacona and Others

Follow-up and Recovery

Patient LF showed a complete recovery 13 months after the first examination.Since in the first assessment the structural description of living categories wasspared, and the semantic deficit on the questionnaire was very mild, we thinkthat the main problem of LF was the activation of phonological units fromsubstantially spared semantic representations, and that this activation eventuallyrecovered, though remaining possibly slower as shown by fluency tasks.

On the contrary, after 20 months EA was still severely impaired, thoughshowing some improvement on naming and answering the questionnaire, limitedto non-living things, and on pointing to pictures for all stimuli. In this patient,who presented with a more severe semantic knowledge degradation, namingimprovement paralleled that of semantic memory (Figure 4) and the improvementitself showed a category dissociaton.

Why did our patients show a marked difference in the recovery? Let us firstconsider the functional aspects. EA presented a considerable central semanticdeficit, whereas LF presented only a slight semantic impairment. We wouldsuggest that a substantial integrity of the semantic system is necessaryfor therecovery of naming, although it may be not sufficient to determine a definiteimprovements as shown by cases where the semantic system is spared but outputphonological representations are lost. The discrepant recovery of differentcategories could be explained with the same hypotheses that we have advocatedelsewhere for the greater vulnerability of living things at onset, i.e. the lesserdegree of correlation between perceptual and functional aspects within livingcategories (Laiacona, Barbarotto and Capitani, 1993; De Renzi and Lucchelli,1994; Capitani et al., 1994). The lack of coherence between functional andvisual attributes in living things is likely to require greater space for storingsemantic units and greater work for the cognitive system in the activation andretrieval of the different facets of living category item representation.

Anatomical Correlates of Semantic Deficits

The lesions of LF and EA are consistent with the data generally reported forpatients presenting the typical category dissociation, i.e., a lesion of the basalstructures of the temporal lobes. However, the anatomical correlates of thissyndrome should be investigated at a more detailed level, and, here, the study of our patients may add relevant data.

The lesions of our patients were far more severe on the left side, and this is consistent with the fact that their deficit was mainly verbal, as judged fromthe lesser involvement of the structural description system. Sartori, Job, Miozzoet al. (1993) and Gainotti et al. (1995) suggested that cases affected by bilaterallesions present not only verbal deficits, but also impairment of the structuraldescription system. In our cases, there was a minor lesion of right temporalbasal areas and, surprisingly, it was larger in the case of LF, whose structuraldescription system was undamaged: though the slight lesional extent does notallow firm conclusions to be drawn about the role of the basal right temporalregion. Recovery data may be relevant here. EA did not recover knowledge of

Semantic category dissociations in HSE 459

living things, despite a substantially spared right hemisphere, while he showed a partial but definite improvement with non-living things. This suggests that hissemantic knowledge about living categories was almost totally subserved by theleft temporal lobe, whose lesion was highly destructive. Should we conclude,then, that the right hemisphere assists the decoding of non-living categories, butnot that of living categories? Alternatively, it can be held that the left hemisphereis responsible for any type of semantic knowledge, but that the neuralrepresentation of non-living categories is more widespread and can, therefore, be carried out by its spared areas. PET data may help to give a defìnitive answer.

A more detailed analysis of the lesional site within the left temporal lobeprovides cues as to the role played by its components. Limbic structures weremost severely damaged in case LF, who presented a milder deficit and asubstantial recovery. This suggests that the extent of limbic damage does notaccount for the different severity and outcome. The major difference betweenour patients resides in the posterior extent of the left temporal lesion, especiallytowards the upper and middle temporal gyrus. Wernicke area and the loweradjacent temporal neocortex were damaged in EA and spared in LF. Wernickeaphasia on its own does not account for category dissociation, but the posteriorparts of the middle and inferior temporal gyri might be involved in the semanticprocessing of living categories. This could explain the difference between thesevere semantic impairment of EA and the slight deficit presented by LF. Wehave no information about the effect of combined lesions of Wernicke area andbasal temporal areas in HSE, and do not know whether the effects of theselesions are simply additive, or show some kind of interaction. As lesiondescriptions reported in the literature are seldom sufficiently detailed, we believethat the collection of a substantial data base is called for.

Acknowledgements.Dr. Rosemary Allpress revised the English text.

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(Received 24 May 1996: accepted 20 November 1996)

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