Selective Sparing of Verb Naming in a Case of Severe Alzheimer's Disease

NOTESELECTIVE SPARING OF VERB NAMING IN A CASE

OF SEVERE ALZHEIMER’S DISEASE

Gail Robinson1, Martin Rossor2 and Lisa Cipolotti1

(National Hospital for Neurology and Neurosurgery London, 1Department of ClinicalNeuropsychology; 2Dementia Research Group)

ABSTRACT

A patient with severe Alzheimer’s disease (AD) presented with a severe impairment innaming nouns but selective sparing of the naming of verbs. Her impairment in namingnouns was presented across a wide range of categories investigated. To our knowledge, thisis the first case documenting the selective preservation of verb naming in a patient withAD. The implications for the notion of an intrinsic vulnerability of verb naming in AD andfor the current knowledge of anatomical correlates of noun/verb processing are discussed.

Key words: Alzheimer Disease, naming, verbs

INTRODUCTION

Several studies of aphasic patients have shown that brain damage can selectively affectspecific categories of grammatical words, such as verbs and nouns. A number of patientshave been reported who show a disproportionate difficulty in producing verbs in the contextof a relatively spared ability to produce nouns (e.g. Caramazza and Hillis, 1991; Daniele,Giustolisi, Silveri et al., 1994; McCarthy and Warrington, 1985; Orpwood and Warrington,1995; Rapp and Caramazza, 1998; Silveri and Di Betta, 1997). Further, it has been reportedthat a selective deficit in the processing of a single grammatical category, verbs, can berestricted to a single modality of output (e.g. Caramazza and Hillis, 1991; Rapp andCaramazza, 1998). Patients with the opposite type of impairment, namely a relatively sparedability to produce verbs in the context of a selective impairment in producing nouns havealso been reported (e.g. Berndt, Haendiges and Wozniak, 1997; Breen and Warrington,1994; Daniele et al., 1994; Hillis and Caramazza, 1995; Silveri and Di Betta, 1997; Zingeserand Berndt, 1988). Three case studies have focused on investigating the extent of the deficitfor nouns (Denes, Meneghello, Vallese et al., 1996; De Renzi and Pellegrino, 1995; Miozzo,Soardi and Cappa, 1994). The noun impairment was found to be pervasive with patientsreported to have profound difficulty across a large number of categories (animals, objects,fruits and vegetables, foods, body parts and famous people’s names). Interestingly, the onlyother category that was relatively spared in all three cases was colours (Denes et al., 1996;De Renzi and Pellegrino, 1995; Miozzo et al., 1994).

Recently, a few studies have specifically investigated the ability to process verbs andnouns in patients with mild to moderate Alzheimer’s Disease (AD) (Cappa, Binetti, Pezziniet al., 1998; Robinson, Grossman, White-Devine et al., 1996; White-Devine, Grossman,Robinson et al., 1996). AD patients were consistently reported to be significantly worse atnaming verbs than nouns even when the frequency of the target verbs and nouns wascontrolled for. This impairment in naming verbs was found to be underpinned by a moregeneral word comprehension deficit (White-Devine et al., 1996). On a spoken word-picturematching task AD patients’ performance was poorer for verbs than nouns. This selectiveimpairment in naming verbs was interpreted as partly due to a semantic memory impairmentwhich is well known to occur in AD (e.g. Hodges, Salmon and Butters, 1992). It has been

Cortex, (1999) 35, 443-450

proposed that a semantic memory impairment in the AD population would have a greaterimpact on processing verbs than nouns. This is because verb meanings are thought to beless redundant, more sparse and less hierarchical than the representations of nouns(Robinson et al., 1996). This hypothesis clearly predicts that in AD patients the ability toname verbs becomes impaired before that of nouns.

In this paper we describe a patient with severe AD who exhibited a remarkably selectivesparing of the ability to name verbs in the context of a severe impairment in the ability toname nouns. As far as we are aware selective sparing of verbs in the context of AD has notbeen previously documented. The implications of this finding for the hypothesis predictingthat verb naming should become impaired before that of nouns in AD are discussed.

CASE REPORT

The patient, a 79-year-old female, right handed, retired health worker was referred tothe Cognitive Disorders Clinic for assessment of progressive memory impairment. Thisstarted five years previously with mislaying items. More recently she developed wordfinding difficulties together with impairment of writing and reading. She had remainedindependent and was able to manage some shopping and housework. She had sustained ahead injury when young but had no other significant past medical history. A younger brotherof five siblings had been diagnosed with Alzheimer’s disease. Neurological examinationwas normal apart from the cognitive impairment described below. On the Mini-MentalState Examination her performance was severely impaired (7/30). A CT scan had shownextensive cerebral atrophy, particularly of medial temporal lobe structures, together withmodest white matter changes but no obvious lacunae. A clinical diagnosis of probableAlzheimer’s Disease was made acording to the NINCDS-ADRDA criteria (McKhann,Drachman, Folstein et al., 1984).

Neuropsychological Assessment

On a shortened version of the WAIS-R her Verbal and Performance IS were in theborderline defective range (VIQ = 71, PIQ = 73). She was disoriented in time and placeand on an easy Recognition Memory Test her performance was at chance (Words = 12/25,Faces = 11/25; Clegg and Warrington, 1994). She was unable to provide either solution tothe Weigl Colour Form Sorting Test (1941).

Language Assessment

Her spontaneous speech was well articulated with normal prosody. No phonological orsyntactic errors were present. The most notable feature was a grave nominal dysphasia. Hernarrative skills were assessed with the Cookie Theft Picture Description Task whichrequired her to produce a verbal description of a drawing of a domestic scene (Goodglassand Kaplan, 1976). The main features were marked word finding difficulties and frequentpauses while she searched for words which resulted in aborted phrases. She made neithersyntactic nor phonological errors. Her responses were analysed in terms of the number ofcontent words and verbs produced. Remarkably, the patient showed a general reduction inher production of content words (4.6% of total words produced) while still being able toproduce numerous verbs (41.5% of total words produced).

Her confrontation picture naming skills were severely impaired. She failed to name anyobjects from the Graded Naming Test (0/30; McKenna and Warrington, 1980) and wasonly able to name two pictures from the Oldfield Picture Naming Test (2/30; Oldfield andWingfield, 1965). By comparison her word comprehension skills were relatively preserved.She performed at an average level on the Vocabulary subtest of the WAIS-R (age scaledscore = 9). Her reading skills as assessed by the National Adult Reading Test (Nelson andWillison, 1991) and the Schonell Graded Word Reading Test (1942) were poor (5/50 and31/100, respectively). Errors were predominantly word substitutions that were either visuallysimilar (e.g. supperfor summer) or semantically related (e.g. drink for thirsty).

444 Gail Robinson and Others

Summary

Formal neuropsychological assessment documents a severe global cognitive impairment.The most prominent feature of the patient’s language impairment was a pronounced nominaldysphasia.

EXPERIMENTAL INVESTIGATIONS

It was noted that although our patient was profoundly anomic she was still able toproduce a considerable number of verbs when describing the Cookie Theft Scene.Furthermore, despite being almost completely unable to name the majority of the picturesfrom the Oldfield Picture Naming Test, she often retrieved an associated verb whenattempting to name the pictures (75% to her incorrect responses; e.g. puff for cigarette,counting for metronome, cut for scissors). In order to explore these observations thefollowing investigations were undertaken.

Test 1. Oral Naming, Reading and Repetition of Verbs and Nouns

In this experiment a task was developed which permitted a thorough investigation ofthe patient’s ability to process verbs and nouns.

Materials

There were 40 black and white line drawings of verbs that all led to concrete actionsand 40 black and white line drawings of objects. Target words were frequency matched(Kucera and Francis, 1982; verbs mean = 27.7, nouns mean = 28.6; Mann-Whitney U = 736.5, p = 0.5405).

Procedure

There were three experimental conditions which were completed in one session in thefollowing order: (1) oral picture naming; (2) reading aloud; and (3) repetition. The samestimuli were used in each condition. In the oral naming task each picture was individuallypresented and the patient was asked to name the action or object depicted. Verbs werepresented first followed by nouns. Responses were marked correct or incorrect. In thereading aloud task the target words were presented in large print in list form with verbspresented first. In the word repetition task the examiner said each word once and the patientwas asked to repeat each stimulus. Nouns were presented first.

Results

The number of correct responses for each condition for both categories were presentedin Table I. A differential effect for both category and condition was demonstrated. Her oralnaming performance was relatively spared for verbs. In contrast, her oral namingperformance was severely impaired for nouns. This difference was highly significant (χ2

[1] = 31.26, p < .0001). Her performance on the reading aloud and repetition tasks for bothverbs and nouns was virtually at ceiling.

Comment

The patient’s ability to name verbs was far superior to her ability to name nouns. Thefact that she could read and repeat verbs and nouns flawlessly ruled out the possibility thather oral naming impairment could be underpinned by some peripheral deficits at the levelof articulating a phonemic sequence.

Sparing of verbs in Alzheimer’s Disease 445

Test 2. Oral Naming of Different Categories; Verbs, Colours, Objects, Animals, Body Parts and Maps

The results of Test 1 indicated that our patient’s performance was characterised bycategory-specific preservation. Her ability to name verbs was far superior to her ability toname nouns. In this experiment we explored the patient’s residual naming skills further.

Materials

The stimuli used in this oral picture naming test were all very common items. Therewere 30 black and white line drawings depicting action verbs (e.g. a person sleeping) thatwere primarily high in frequency (23 A and AA Thorndike-Lorge and 7 items ranging from5-44). There were 50 coloured pictures comprising 10 highly familiar items (frequency ofA and AA Thorndike-Lorge) from each of the following 5 categories; colours (e.g. red),objects (e.g. cup), animals (e.g. dog), body parts (e.g. eye), and maps (e.g. England) (thestimuli from these 5 categories were partly based on the test used by McKenna andWarrington, 1978).

Procedure

The test was administered in two sessions on two days; verbs were tested in the firstsession and the remaining 5 categories were tested in the second session. The stimuli werepresented in blocks that contained all of the items in each category. The patient was askedto name the corresponding action or the item depicted. Responses were marked correct orincorrect.

Results

The number of correct responses for each category is presented in Table II. Thepatient’s ability to retrieve the names of verbs was remarkably well preserved. It is notablethat 95% of her correct responses were inflections of the target (e.g. clapping for clap). Bycontrast her ability to retrieve the names of items from the 5 categories was profoundlyimpaired. No significant category effects were found for the 5 categories (χ2 [4] = 7.46,n.s.). Naming of colours was only marginally better than naming of items from the other 4 categories.

Comment

The results obtained provide further evidence for a strong selective sparing of thepatient’s ability to name verbs orally. Her oral naming skills were severely impaired acrossa number of other categories of nouns.


TABLE I

Verbs and Nouns: Number and Percentage Correct

Verbs Nouns

Oral naming 32/40 7/40(80%) (17.5%)

Repetition 40/40 39/40(100%) (97.5%)

Reading 38/40 38/40(95%) (95%)

Test 3. Comprehension of Verbs and Nouns

The results of the previous 2 tests demonstrated that the patient presented with aselective sparing in the oral naming of verbs. In order to investigate whether her impairednoun naming was underpinned by a deficit at the level of meaning, a stringentcomprehension test using low frequency verbs and nouns was designed.

Materials

Comprehension of verbs was tested with a stringent written two-choice synonym test (arevised version of the test devised by Manning and Warrington, 1996). Noun comprehensionwas tested using a similar stringent written two-choice synonym test (Warrington, McKennaand Orpwood, 1998).

Procedure

The test was administered in the following order; (1) nouns and (2) verbs. All stimuliwere presented in a written format and spoken aloud by the examiner. KIT was required tochoose the word that was synonymous with the target from the two alternatives provided(e.g. ACQUIESCEmeans agreeor acquire; VIADUCT means damor bridge).

Results

The patient’s performance on the verb synonym test was almost identical to that of 5age- and education-matched controls (23/27; mean = 23.6, SD = 3.97). By contrast, herperformance was severely impaired for nouns (31/50; 5th pecentile).

Comment

The results from these tasks suggest that the patient’s impairment in naming nouns wasunderpinned by a deficit at the level of word comprehension. By contrast, her ability tounderstand verbs was well preserved.

DISCUSSION

This study describes an investigation of the residual oral naming skills of a patient withsevere clinically diagnosed AD. The patient had a profound anomia for a wide variety ofcommon nouns. Her performance on tasks requiring her to name colours, objects, animals,body parts and maps was extremely poor. In sharp contrast she presented with a sparedability to name verbs. On verb naming tasks her performance was remarkably good.Furthermore, when she attempted to name nouns she frequently resorted to retrieving anassociated verb instead. The grave impairment in retrieving nouns was underpinned by adeficit at the level of the semantic representations. The patient’s comprehension of nounswas impaired on a stringent synonym task. In contrast, her performance was well within


TABLE II

Oral Naming of Different Categories: Number and Percentage Correct

Number correct % correct

Verbs 21/30 70Colours 5/10 50Objects 1/10 10Animals 1/10 10Body parts 3/10 30Maps 1/10 10

the control range on a stringent verb synonym task. It was of interest to note that herselective sparing of verb naming was not associated with a similar sparing of colour naming.Her performance in naming colours was only marginally better than her naming of itemsfrom other categories. However, her colour naming was clearly much poorer than herperformance for verbs, especially if one considers that the verb names were lower infrequency than the colour names. In the aphasic literature several patients reported with aselective sparing of verbs also presented with a selective preservation of colour naming(e.g. Denes et al., 1996; De Renzi and Pellegrino, 1995; Miozzo et al., 1994). The findingsin our patient indicate that the selective sparing of verbs can occur independently from theselective sparing of colours. Thus, the reported pattern of association between verb andcolour sparing may simply reflect the adjacency of the neuronal substrata.

To our knowledge, the patient is the first reported case in the AD literature who presentswith the selective sparing of the naming of verbs. Indeed, recent studies of patients withmild to moderate AD have documented the opposite pattern of impairment, that is, a greaterimpairment of the naming of verbs relative to nouns (Cappa et al., 1998; Robinson et al.,1996; White-Devine et al., 1996). These results were interpreted as indicating an increasedvulnerability of verbs to a degradation in semantic memory. In particular in the Robinsonet al., and White-Devine et al. studies, the selective verb impairment was accounted for interms of the Miller and Fellbaum (1991) conceptualisation of word meanings. According tothis theory the meanings of nouns and verbs are underpinned by their own set of “semanticrelations” or “organisational structure”. This is determined by the different role they play inlanguage processing. Nouns are described as underpinned by semantic relations; they areconceptualised as having a strong hierarchical taxonomic organisation that offers muchredundancy. By contrast, the semantic relations underpinning verbs are described as muchshallower, more sparse and less redundant. Thus, according to this theory, the relativelysparse semantic relations of verbs will render them more vulnerable than nouns to thesemantic impairment in AD. In the study of Cappa et al. (1998), it was hypothesised thatAD affects the verb category to a greater extent because this is an “...extremely complexand heterogeneous grammatical category...”, p. 353).

Both formulations imply that a selective preservation of verbs should not be observedin AD. The findings in our case would argue for the contrary and suggest that rather thanan intrinsic vulnerability of verbs in AD, word knowledge is organised by grammaticalcategory with separate brain structures subserving the processing of verbs and nouns (e.g.Caramazza et al., 1994; Damasio and Tranel, 1993; Hillis and Caramazza, 1991).

If word knowledge is organised by grammatical category with separate specialised brainstructures, then what might be the possible cognitive basis for the neuroanatomicalseparation of verb and noun knowledge? It has been proposed that differences in the waythat particular categories are acquired in childhood might determine the way that they arestored and encoded in the brain (e.g. Warrington and McCarthy, 1987). Experimental workwith infants has served to emphasise just how different verbs are from other types of lexicalknowledge in the process of language acquisition (e.g. Gleitmen, 1994). Thus, it is possibleto speculate that the dissociation between verbs and nouns might reflect their differingdependencies on specialised processing channels integrating motor and sensory information.During acquisition verbs are presumably closely linked with sensorimotor schema of actionswith a critical contribution from efferent motor channels (e.g. Gainotti, Silveri, Daniele etal., 1995). By contrast, acquisition of nouns might be more reliant on the integration ofsensory inputs. Following this distinction, the sparing of verbs in our patient might beexplained as a consequence of the sparing of the specialised neuronal systems whichrepresent and compute sensorimotor schema of action information. In this context, it isnoteworthy that all the verbs used in the naming tasks were action verbs.

What is the neurological basis of the sparing of verbs in AD? In the literature it isoften reported that verbs are represented in the left frontal region and nouns in the leftanterior and middle temporal regions (e.g. Breedin and Martin, 1996; Damasio and Tranel,1993; Daniele et al., 1993; Gainotti et al., 1995; Miozzo et al., 1994; Zingeser and Berndt,1988). However, there are exceptions; for example, De Renzi and Pellegrino (1995)described a patient in whom verbs were more preserved that nouns following an extensivelesion in the left premotor cortex. Similarly patients have been reported who showed a


greater impairment in the production of verbs than nouns, following lesions limited to theleft temporal and parietal areas (e.g. Caramazza and Hillis, 1991; Miceli, Silveri, Nocentiniet al., 1988). Thus, the anatomical substrata of the verb/noun dissociation is far from beinga resolved issue. Our patient was assessed when CT neuroimaging already showedextensive cortical atrophy, albeit with a temporal lobe emphasis and so no conclusiveargument can be made concerning the anatomical correlates of her spared verb processingability.

In conclusion, this study documented the selective sparing of verb naming in a patientwith severe AD. This data challenges recent reports suggesting that mild to moderate AD isassociated with a category-specific deficit in the naming of verbs. Clearly, the patientdemonstrates that this is not always the case. The selective sparing of verbs in AD reportedhere taken together with the previously reported selective impairment of verbs in AD iscompatible with the known heterogeneity in the clinical presentation of AD. The fact thatin our patient, the processing of verbs remained intact in the midst of a severe cognitiveand language impairment suggests that verbs are processed by an information encapsulatedpathway distinct and separable from that involved in processing nouns.

Acknowledgement. We thank Ms. L. Farquharson for collecting the control data.

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(Received 25 September 1998; accepted 15 December 1998)


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Selective Sparing of Verb Naming in a Case of Severe Alzheimer's Disease