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A Neural Basis for the Retrieval ofWords for ActionsDaniel Tranel , Ralph Adolphs , Hanna Damasio & Antonio R.DamasioPublished online: 09 Sep 2010.

To cite this article: Daniel Tranel , Ralph Adolphs , Hanna Damasio & Antonio R. Damasio(2001) A Neural Basis for the Retrieval of Words for Actions, Cognitive Neuropsychology, 18:7,655-674

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A NEURAL BASIS FOR THE RETRIEVAL OF WORDSFOR ACTIONS

Daniel Tranel and Ralph AdolphsUniversity of Iowa College of Medicine, Iowa City, USA

Hanna Damasio and Antonio R. DamasioUniversity of Iowa College of Medicine, Iowa City and The Salk Institute for Biological Studies, La Jolla, USA

Although much has been learned in recent years about the neural basis for retrieving words denotingconcrete entities, the neural basis for retrieving words denoting actions remains poorly understood. Weaddressed this issue by testing two specific anatomical hypotheses. (1) Naming of actions depends notonly on the classical implementation structures of the left frontal operculum, but also on mediationalstructures located in left premotor/prefrontal areas. (2) The neural systems subserving naming ofactions and naming of concrete entities are segregated. The study used the lesion method and involved75 subjects with focal, stable lesions in the left or right hemispheres, whose magnetic resonance datawere analysed with a three-dimensional reconstruction method. The experimental tasks were standard-ised procedures for measuring action and object naming. The findings offered partial support for thehypotheses, in that: (1) lesions related to impaired action naming overlapped maximally in the left fron-tal operculum and in the underlying white matter and anterior insula; and (2) lesions of the left anteriortemporal and inferotemporal regions, which produce impairments in naming of concrete entities, didnot cause action naming deficits. A follow-up analysis indicated that action naming impairments, espe-cially when they were disproportionate relative to concrete entity naming impairments, were not onlyassociated with premotor/prefrontal lesions, but also with lesions of the left mesial occipital cortex andof the paraventricular white matter underneath the supramarginal and posterior temporal regions.

INTRODUCTION

We previously reported a double dissociationbetween naming of concrete entities and naming ofactions, whereby the former was associated with theleft inferotemporal region, and the latter with theleft prefrontal region (A.R. Damasio & Tranel,1993; Fiez, Damasio, & Tranel, 1996; Tranel,Damasio, & Damasio, 1997b, 1998). We found

that lesions in the left frontal operculum, involvingboth prefrontal and premotor cortex and underly-ing white matter, were associated with defectivenaming of actions and normal naming ofnonunique concrete entities such as animals andtools; by contrast, left inferotemporal lesions wereassociated with defective naming of concrete enti-ties, but normal naming of actions. The lesionsassociated respectively with defective action nam-

COGNITIVE NEUROPSY CHOLOGY, 2001, 18 (7), 655–670

Ó 2001 Psychology Press Ltdhttp://www.tandf.co.uk/journals/pp/02643294.html DOI:10.1080/02643290143000015

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Requests for reprints should be addressed to Daniel Tranel, PhD, Department of Neurology, University of Iowa Hospitals andClinics, 200 Hawkins Drive, Iowa City, Iowa 52242, USA (Tel: 319/2384-6050; Fax: 319/356-4505;Email: [email protected]).

This study was supported in part by a grant from the National Institute for Neurological Diseases and Stroke (Program ProjectGrant NS 19632). We thank Dr David Kemmerer for many helpful comments on the manuscript, Drs Julie Fiez and Greg Cooper forhelp with earlier phases of this project, and Ken Manzel, Ellen Steffensmeier, Jon Spradling, Denise Krutzfeldt, and Kathy Jones forexpert technical help.

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ing and defective concrete entity naming werenonoverlapping; thus, there was a double dissocia-tion relative to naming performance and site oflesion. Subsequently, comparable dissociationshave been reported by other investigators (Daniele,Giustolisi, Silveri, Colosimo, & Gainotti, 1994;Miozzo, Soardi, & Cappa, 1994), and recent func-tional imaging (H. Damasio et al., in press; Koeniget al., 1999; Perani et al., 1999; Warburton et al.,1996) and electrophysiological studies (Dehaene,1995; Pulvermuller, Lutzenberger, & Preissl, 1999)have begun to provide some convergent evidence.These findings suggested that the systems requiredfor retrieval of words for concrete entities andretrieval of words for actions1 are, at least in part,segregated in the human brain, even if they nor-mally operate in coordinated fashion.

This pattern of neuropsychological dissociationis in keeping with a number of studies in which themain thrust was typically the distinction of differentpatterns of linguistic deficits in patients with apha-sia (Breedin & Martin, 1996; Caramazza & Hillis,1991; Daniele, Silveri, Giustolisi, & Gainotti,1993; Goodglass, Klein, Carey, & Jones, 1966;Hillis & Caramazza, 1995; McCarthy &Warrington, 1985; Miceli, Silveri, Nocentini, &Caramazza, 1988; Miceli, Silveri, Villa, &Caramazza, 1984; Zingeser & Berndt, 1988, 1990)or dementia (Cappa et al., 1998; Funnell &Hodges, 1991; Robinson, Grossman, White-Devine, & D’Esposito, 1996; Snowden, Griffiths,& Neary, 1996) (for reviews, see Gainotti, Silveri,Daniele, & Giustolisi, 1995; Grossman, 1998;Saffran & Sholl, 1999). For example, Goodglass,Christiansen, and Gallagher (1994) compared theproductions of agrammatic aphasics (usuallyBroca’s) and conduction aphasics. Consistent withprevious studies of this type (Marin, Saffran, &Schwartz, 1976; Miceli, Mazzuchi, Menn, &Goodglass, 1983; Myerson & Goodglass, 1972),the authors found that agrammatic aphasics had apreponderance of nouns over verbs in runningspeech and in single-constituent utterances. This

finding is also consistent with other reports ofnoun-verb discrepancies in word repetition (Katz& Goodglass, 1990) and written word retrieval(Caramazza & Hillis, 1991).

We have interpreted the evidence adduced fromthese studies in the context of a theoretical frame-work in which we see actual word-form productionas dependent on three kinds of neural structures: (1)structures that support conceptual knowledge (dis-tributed in early and high-order sensory cortices ofboth hemispheres and in some subcortical nuclei);(2) structures that support the implementation ofword-forms in eventual vocalisation (the classicallanguage areas located in the left perisylvian region,including Broca’s area); and (3) mediational struc-tures, which are partially separable from the othertwo kinds of structures, and which are engaged bythe structures in (1) to trigger and guide the imple-mentation process executed in (2). Mediationalstructures are found outside the classical language-related areas; examples include, for the case of con-crete entity naming, areas in inferotemporal (IT)and temporal-polar (TP) cortices. The notion of anintermediary step interposed between semanticsand output phonology has also been incorporated insome cognitive linguistic models (e.g., Gordon,1997; Levelt, Roelofs, & Meyer, 1999), although itis important to note that our framework is builtaround the neural, rather than cognitive, compo-nents of these processes.

The rationale and layout of this framework havebeen discussed elsewhere (e.g., A.R. Damasio,1989; A.R. Damasio & Damasio, 1994; A.R.Damasio, Damasio, Tranel, & Brandt, 1990; H.Damasio, Grabowski, Tranel, Hichwa, &Damasio, 1996; Tranel, Damasio, & Damasio,1997a, b). Briefly, we note that: (1) the architecturewe propose is not constituted by rigid “centres” and“pathways,” but rather, by flexible neuron ensem-bles interconnected by flexible bidirectional path-ways; (2) the primary shaping of those neuronensembles and pathways is due to evolutionaryhistory and is transmitted genomically; and (3) the

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656 COGNITIVE NEUROPSYCHOLOGY , 2001, 18 (7)

1 We note that words for actions are often referred to as “verbs,” although it is important to emphasise that we are concerned withthe processing of word-forms only, rather than the complex set of lexical information implied by the term “verb” (cf., Fromkin &Rodman, 1998; Jackendoff, 1990; Pinker, 1989).

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secondary shaping is carried out by learning, thusaffording considerable individual neuroanatomicaland neurophysiological differences. The retrieval oflinguistic knowledge required to reconstruct thesensorimotor patterns on the basis of which word-forms become explicitly represented in mind,occurs in temporally correlated fashion, withinappropriate early sensory cortices (e.g., auditory,visual, somatosensory) and motor structures of theimplementation regions. Those patterns are trig-gered by relevant mediational circuits, which con-stitute a third-party step between retrieval ofconceptual knowledge and retrieval of word-forms.The sensorimotor patterns that embody the explicitrepresentations of word-forms do not occur at themediational circuitry sites. The actual operation ofthis neural architecture is probability-driven anddepends on the circumstances of the organism—forinstance, the demands of a given task and the par-ticular conditions of a given individual. Moreover,the ensembles and pathways hypothesised to sup-port a particular function, say, the retrieval of wordsfor a certain class of concepts, are seen as “preferredsystems” rather than as “single-and-only” systems,i.e., we presume that certain systems support themost efficient, effective, and complete version of acertain performance, but we imagine that there areother systems that can support parts of the perfor-mance, albeit not necessarily as efficiently. Finally,we note that the systems outlined here are a simpli-fication meant to serve as a basis for testable neuro-anatomical hypotheses. We see this three-partanatomical account as a step in the enterprise ofexploring functional anatomy, and we note that ouraccount, which is neurally grounded, is not offeredas an alternative to models of word productionwhich have a primary or exclusive basis on cognitivearchitectures (e.g., Caramazza, 1997; Levelt et al.,1999).

In the current study, we tested the followinghypotheses: (1) naming of actions depends not onlyon the implementation structures of the left frontaloperculum, but also on mediational structureslocated in the left premotor/prefrontal areas; and(2) the neural systems subserving naming of actionsand naming of concrete entities are segregated.Specifically, we predicted that (2a) lesions associ-

ated with impaired action naming would sparenaming of concrete entities; and that (2b) lesionsassociated with impaired naming of concrete enti-ties—namely, in left anterior temporal andinferotemporal regions—would not impair namingof actions. We tested these hypotheses in a prospec-tive experiment, using the lesion approach in a largegroup of subjects. The latter two predictions wereaddressed by investigating naming performancesfor several categories of concrete entities (faces, ani-mals, tools) and contrasting them with naming per-formance for actions.

METHOD

Subjects

Seventy-five subjects with circumscribed unilateralleft (N = 54) or right (N = 21) hemisphere braindamage were selected from the Patient Registry ofthe University of Iowa’s Division of CognitiveNeuroscience. All gave informed consent in accor-dance with the Human Subjects Committee of theUniversity of Iowa. As a group, the subjects’ lesionspermitted us to probe most of the left hemisphereand a substantial part of the right hemisphere.Lesions were due to cerebrovascular disease (N =61), temporal lobectomy (N = 12), or herpes sim-plex encephalitis (N = 2). To be eligible for thestudy, subjects had to have lesions that could beanalysed with our MAP-3 technique (see below).Handedness, measured with the Geschwind-Oldfield Questionnaire, which has a scale rangingfrom complete right-handedness (+100) to com-plete left-handedness (–100), was distributed asfollows: 69 subjects were fully right-handed (+90or greater), 3 were primarily right-handed (+80, +70, +55), 2 were fully left-handed (–90, –100), and1 was primarily left-handed (–60). Neurological,neuropsychological, and, for the temporallobectomy cases, neurosurgical (WADA testing)data indicated that all subjects had left-hemispherelanguage dominance. The average age of the sub-jects was 52.7 years (range = 20–87; SD = 17.1).

The subjects had been extensively characterisedneuropsychologically and neuroanatomically,

COGNITIVE NEUROPSYCHOLOGY, 2001, 18 (7) 657

RETRIEVING WORDS FOR ACTIONS

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according to standard protocols (H. Damasio &Damasio, 1989; H. Damasio & Frank, 1992;Frank, Damasio, & Grabowski, 1997; Tranel,1996). All subjects had normal intelligence (asmeasured by the WAIS-R/WAIS-III); a highschool level of education or higher; no difficultyattending to or perceiving visual stimuli; and allsubjects were able to give valid verbal responses.Many of the subjects with left-hemisphere lesionswere recovered aphasics; however, in none of themdid the residual aphasia preclude the production ofscorable responses (subjects rarely failed to produceany response to a stimulus, and we did not observeany relationship between “no response” error typesand degree of residual aphasia, see Kemmerer &Tranel, 2000b). All subjects were studied in thechronic phase of recovery, i.e., 3 months or moreafter lesion onset; the average time post-lesiononset was 5.9 years (SD = 4.6).

Stimuli and procedures

The task we used for measuring retrieval of wordsfor actions was the Action Naming Test, which wasdeveloped and standardised in our laboratory (Fiez& Tranel, 1997). The test comprises colour photo-graphs of various actions, and the items elicitresponses that vary along several dimensions,including: (1) the inflection (tense/aspect) of theelicited response, (2) the frequency of the elicitedverb per million words (Francis & Kucera, 1982),(3) the type of agent performing each action (per-son, animal, or object), and (4) compatability withdifferent argument structures (for details, see Fiez& Tranel, 1997, and Kemmerer & Tranel, 1998,2000a). The items also represent a diverse range ofconceptual categories (e.g., verbs of perception,motion, etc.), insofar as these can be specified forverbs (cf., Miller & Fellbaum, 1991; Kemmerer &Tranel, 2000a, b).

The Action Naming Test comprises 100 items.Seventy-five of the stimuli are single picturesdepicting an ongoing action, designed to elicitverbs in the imperfective aspect (e.g., “walking”).The remaining 25 stimuli are picture pairs depict-ing some change in an object, designed to elicitverbs in the perfective aspect (e.g., “chopped”).

Detailed instructions for the test administration areavailable in Fiez and Tranel (1997; see Experiments1 and 2). In brief, this entailed the following: Foritems consisting of a single picture, the subject wastold to say a single word that best described what theperson, animal, or object was doing. For items con-sisting of a picture pair, the subject was told that thepicture on the left depicted a person or object beforesome action, and the picture on the right depictedthat person or object after some action. The subjectwas told to say a single word that best described whatwas done to each object, or what each person orobject had done.

Since this study was designed as an initial,broad-based effort to identify neural correlates ofaction word retrieval, we did not formulate or testspecific predictions regarding various verb types. Inparticular, we are not concerned here with adetailed analysis of potential differences betweenimperfective and perfective verb forms. For the pur-poses of this study, after finding that scores onimperfective versus perfective items tended to behighly correlated, we collapsed across this distinc-tion and analysed all action naming responsestogether. Also, we do not deal here with other dis-tinctions among verb types, e.g., conceptual cate-gory or type of agent, as this issue is beyond thescope of the current study. For a detailed analysis ofthis topic from a neuropsychological perspective,the reader is referred to Kemmerer and Tranel(2000a).

Measurement of retrieval of words for concreteentities was conducted using standard proceduresand stimuli described previously (H. Damasio et al.,1996; Tranel et al., 1997a, b, 1998). We studiednaming performances in three categories—faces,animals, and tools. (These categories were chosenbecause they have been extensively investigated inprevious work, and hence constitute a solid basis forcomparison.) The stimuli were black-and-whitephotographs or line drawings of famous faces (N =133), animals (N =90), and tools (N =104); many ofthe animal and tool stimuli were drawn from theSnodgrass and Vanderwart (1980) set. The mainobjective in the current study was to investigateneural correlates of action naming, and to explorethe specificity of this relationship; hence, we

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utilised here a subset of the subjects studied previ-ously in connection with our work on concreteentity naming (H. Damasio et al., 1996; Tranel etal., 1997b, 1998).

For the action stimuli, and for the concreteentity stimuli from the categories of animals andtools, we calculated average values for a number ofstimulus characteristics that may influence recogni-tion and naming performance, including wordlength, word frequency, name agreement, imageagreement, familiarity, and visual complexity (cf.,Humphreys, Riddoch, & Price, 1997; Laws &Neve, 1999; Tranel, Logan, Frank, & Damasio,1997c). Word length refers to the number of lettersin the name of an item. Word frequency is based onthe values provided in Francis and Kucera (1982).Name agreement refers to the percentage of sub-jects who produced the same name for a particularstimulus. Image agreement is a rating of the extentto which each picture matched subjects’ mentalimage of the item. Familiarity is a rating of howcommon or usual the stimulus is in subjects’ normalrealm of experience. Visual complexity is a rating ofhow much visual detail or intricacy is in a picture.The name agreement, image agreement, familiar-ity, and visual complexity ratings were taken fromthe published values in Snodgrass and Vanderwart(animals, tools) and Fiez and Tranel (actions).Although the values for animals/tools and foractions were derived from different normative pop-ulations, it should be noted that the variables weredefined and operationalized in the same manneracross all three categories (see Fiez & Tranel, 1997;Snodgrass & Vanderwart, 1980).

Data regarding these six stimulus variables areprovided in Table 1. To examine between-categorydifferences, a one-way ANOVA was performed oneach of the variables, using category (animals, tools,actions) as the grouping variable. All of these weresignificant: word length, F(2) = 15.93, p < .001;word frequency, F(2) =6.05, p< .005; name agree-ment, F(2) =6.87, p< .005; image agreement, F(2)

=11.81, p< .001; familiarity, F(2) =38.49, p< .001;visual complexity, F(2) = 71.03, p < .001. Duncanmultiple-range follow-up tests indicated that forword length, action words were longer than animaland tool names; for word frequency, action wordswere more frequent than animal and tool names; forname agreement, action words had lower agree-ment than animal and tool names; for image agree-ment, animal stimuli were lowest, tool stimuli wereintermediate, and action stimuli were highest; forfamiliarity, tools were the most familiar, actionswere intermediate, and animals were the leastfamiliar; for visual complexity, animals were higherthan actions and tools.

These results indicate that although the catego-ries are not “matched” on these different stimulusvariables2, there is no systematic pattern of higheror lower rankings that distinguishes one categoryfrom the others. Factors that have been purportedto influence the success of word retrieval weremixed across categories; for instance, animals hadthe highest name agreement, but the lowest famil-iarity; actions had the highest word frequency, butthe lowest name agreement. This outcome, com-bined with the fact that category-related double



Table 1. Average values on stimulus variables for concrete entities(animals, tools) and actions

Category———————————————–

Variable Animals Tools Actions

Word length 5.6 6.2 7.4Word frequency 13.3 34.8 69.2Name agreement 87.5 86.1 77.4Image agreement 3.6 3.9 4.1Familiarity 2.4 3.6 3.2Visual complexity 3.8 2.4 2.5

aWord length refers to the number of letters in the name ofthe stimulus. Word frequency, name agreement, imageagreement, familiarity, and visual complexity were derivedfrom the published values in Snodgrass and Vanderwart(animals, tools) and Fiez and Tranel (actions).

2 We should also note that a priori “matching” of stimulus sets on variables such as these is fraught with its own types of problems,not the least of which is the creation of stimulus sets that contain highly unrepresentative exemplars (see Dixon, Piskopos, &Schweizer, 2000, for a similar critique). And for some factors, matching is simply not feasible (cf., Pulvermuller, Harle, & Hummel,2000).

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dissociations of naming occurred in this and otherexperiments of this type that we have conducted,makes it untenable to explain the results on thebasis of systematic category-related differences inthese stimulus factors.

Neuropsychological data quantification andanalysis

Each subject’s performance on the Action NamingTest was calculated as percentage correct. Scoringof items was based on the normative data from Fiezand Tranel (1997). Specifically, the standardisationyielded, for each item on the test, a namingresponse (or in a few instances, two or threeresponses) that was considered correct. To quantifythe performances of the brain-damaged subjects,we compared their responses to those of the stand-ardisation sample, and scored as correct thoseresponses that matched those produced by the nor-mal controls. There was one exception: normally,our scoring procedure classifies as errors verbresponses that are not inflected properly (or at all);however, given the objectives of the current study,we scored all responses that contained the base formof the verb as correct, irrespective of whether theinflection was correct. That is, we did not want topenalise subjects for inflection errors, since ourstudy is concerned with word retrieval and not withgrammatical processing. On the other hand, pho-nological errors were scored as incorrect responses.Since phonological errors are of particular signifi-cance in the context of the current investigation,though, we applied a follow-up scoring analysisthat reclassified phonological errors (see following).The primary data analyses utilised the initial scoresderived from the standard scoring protocol (withinflection errors scored as correct).

Data from the 75 brain-damaged subjects wereplotted according to percentage correct scores. (SeePlate 1 situated between pages 656 and 657.) Toexplore whether these scores were drawn from oneor from more than one Gaussian normal distribu-tions, we obtained quantile-quantile plots (actualdata versus the scores that would be expected if the

data were normally distributed, “N-scores”), as fol-lows. Typically, the ith N-score for a sample of sizeN is obtained from the mean of the sampling distri-bution of the ith order statistic in a sample of Nvalues drawn from a standard normal distribution.(In order to increase resistance to skewness, we con-ducted the analysis using the medians of the sam-pling distributions, rather than the means.) The ithmedian order statistic of a sample size N wasapproximated by the function: InvGaussian(i-1/3)/N+1/3), where InvGaussian is the inverse Guassian(or normal) cumulative distribution function.

The resulting plots were piecewise linear,namely, over the ranges of those scores that behavedas if drawn from the same, single distribution (Plate1). We used a dynamic least-squares regression ofactual scores versus N-scores to isolate those scoresthat were most likely to belong to the same distribu-tion. Beginning at each extreme of the score range(the lowest score and the highest score), we calcu-lated the least-squares fit continuously as additionalscores were added, until a maximum was reached.We also applied the more conventional approach ofclassifying subjects as impaired if their scores weretwo or more standard deviations below the mean ofthe control subjects studied by Fiez and Tranel(1997), i.e., if their z-scores were less than or equalto –2.0. We used z-scores to quantify naming per-formances in the concrete entity categories (seebelow).

Neuroanatomical data quantification andanalysis

The neuroanatomical analysis was based on mag-netic resonance (MR) data obtained in a 1.5 Teslascanner with an SPg sequence of thin (1.5 mm) andcontiguous T1 weighted coronal cuts, and recon-structed in three dimensions using Brainvox (H.Damasio & Frank, 1992; Frank et al., 1997). (In afew subjects in whom MR data could not beobtained, the analysis was based on computerizedaxial tomography [CT] data.) All neuroimagingdata were obtained in the chronic epoch (at least 3months post onset of lesion). The final anatomical


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description of the lesion overlap and of its place-ment relative to neuroanatomical landmarks wasperformed with Brainvox, using the MAP-3 tech-nique. All lesions in this set were transposed andmanually warped into a normal 3-D reconstructedbrain, so as to permit the determination of the max-imal overlap of lesions relative to subjects groupedby neuropsychological defect according to themethod specified earlier.

A detailed description of MAP-3 is provided inFrank et al. (1997); in brief, it entails: (1) a normal3-D reconstructed brain is resliced so as to matchthe slices of the MR/CT of the subject and create acorrespondence between each of the subject’s MR/CT slices and the slices of the normal brain; (2) thecontour of the lesion on each slice is then trans-posed onto the matched slices of the normal brain,taking into consideration the distance from theedge of the lesion to appropriate anatomical land-marks; (3) for each lesion, the collection of contoursconstitutes an “object” that can be co-rendered withthe normal brain. The objects in any given groupcan intersect in space, and thus yield a maximaloverlap relative to both surface damage and depthextension. The number of subjects contributing tothis overlap is thus known.

Statistical analysis

To address the first hypothesis—that naming ofactions is associated with left premotor/prefrontalstructures—we grouped subjects according to theirscores on the Action Naming Test, and analysedthe neuroanatomical results. We utilised a lesionanalysis approach that we have used previously oncomparable datasets (Adolphs, Damasio, Tranel,Cooper, & Damasio, 2000). Specifically, we con-trasted the group of subjects who fell in the lowerpartition of the distribution graphed in Plate 1 (N =22; see Results below) with an equal number of sub-jects (N =22) who fell in the upper end of the higherpartition of the distribution. A MAP-3 lesion over-lap was calculated for each group, and then the twoMAP-3 overlaps were contrasted by subtractingone from the other. Thus, neuropsychological per-formance (action naming) served as the independ-

ent variable, and lesion overlap (according toMAP-3) served as the dependent variable. Also, inorder to confirm statistically the reliability of thefindings, we used parametric techniques to com-pare neuropsychological performances in particularsubgroups of subjects (see following).

The lesion subtraction proceeded arithmeticallyfor each brain voxel (see Adolphs et al., 2000, foradditional details about this method). We took thenumber of subjects with high (unimpaired) actionnaming scores (as defined above) who had lesions ata given voxel, and subtracted this from the totalnumber of subjects with low (impaired) actionnaming scores who had lesions at that same voxel.Thus, the subtraction yields a difference in thenumber of lesions at each voxel, reflecting the pro-portion of subjects with low scores, compared withthe proportion of subjects with high scores, whohad damage at that voxel. This arithmetic subtrac-tion of subject numbers was applied to all voxels inthe brain. As shown in Plate 2 (situated between pp.656 and 657), some voxels were not assigned acolour, which means that these are regions of thebrain in which no subject had a lesion.

The two predictions associated with the secondhypothesis were tested as follows. For the first pre-diction—that lesions associated with impairedaction naming would spare naming of concreteentities—we investigated the concrete entity nam-ing performances of subjects who had impairedaction naming, and whose lesions involved struc-tures that were identified as being important foraction naming (according to the analysis used totest the first hypothesis, as indicated earlier). Forthe second prediction—that lesions associated withimpaired naming of concrete entities (left anteriortemporal/inferotemporal) would not impair nam-ing of actions—we explored the extent to whichlesions restricted to the left temporal lobe wereassociated with action naming impairments, usingthe relevant neuropsychological and neuroana-tomical datasets. The justification for focusing onthe left temporal lobe derives from previous work,which has shown that concrete entity naming isrobustly associated with this region (e.g., H.Damasio et al., 1996; see Introduction).



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RESULTS

Defining “impaired” and “unimpaired”action naming performances

Analysis of the distribution of action naming scoresin the 75 brain-damaged subjects, using the least-squares method specified earlier, revealed two dis-tinct populations (Plate 1, situated between pp. 656and 657). We designated the one with the highermean score as “unimpaired,” and the one with thelower mean score as “impaired.” (A z-scoreapproach, in which scores of –2 or lower were classi-fied as impaired, yielded almostexactly the sametwogroups as those identified in the least-squaresmethod, with the single exception that one subjectclassified as “impaired” in the least-squares methodhad a z-score of –1.8.) Action naming scores andhemispheric lesion distributions were as follows: ofthe 22 impaired subjects (mean =54.4, SD =19.1),19 had left-hemisphere lesions and 3 had right-hemisphere lesions. There were 53 unimpaired sub-jects (mean =86.7, SD =6.4); of these, 35 had left-hemisphere lesions and 18 had right-hemispherelesions. As expected given the criterion used to clas-sify thesubjects, a statisticalcomparisonofthescoresof the impaired and unimpaired groups (one-tailedt-test) was highly significant (p< .0001). Also, it isimportant to note that the normal subjects reportedby Fiez and Tranel (1997) achieved an average per-centage correct score of 85.2 (SD = 5.0) on theAction Naming Test; thus, the brain-damaged sub-jects classified as unimpaired in the current studyperformed quite comparably to normal controls.

Testing hypothesis 1

With regard to the first hypothesis, Plate 2 (situ-ated between pp. 656 and 657) shows the MAP-3subtraction result, derived from subtracting thelesion overlaps of 22 unimpaired subjects from thelesion overlaps of the 22 impaired subjects. Thesubtraction revealed a maximal overlap differenceencompassing the left frontal operculum (parstriangularis and opercularis), the inferior sector ofthe precentral and postcentral gyri, and the under-lying white matter and the anterior sector of the

insula. In other words, there were more subjectswith lesions in this overlap region who hadimpaired action naming scores than there were sub-jects who did not. The area of overlap extended intothe depth of the opercular region. On the basis ofthe lesion overlaps for the 22 impaired subjects, a“hot spot” was identified, specifically, a region oflesion overlaps which included at least 7 subjects(Plate 3, situated between pp. 656 and 657). Thishot spot comprises the white matter underlying theleft frontal operculum and the adjoining precentralgyrus, and the anterior insula.

Our next step was to focus specifically on thesubjects with left-hemisphere lesions, given thatthe demands of the task (word retrieval) would beexpected to be associated predominantly with left-hemisphere processing. We examined the mappedlesions of each of the 54 subjects with left-hemi-sphere lesions for possible overlap with the hot spot.In 14 subjects, the lesions overlapped the hot spot,and in 40 the lesions did not. We compared theaction naming performances of these two groupsstatistically (one-tailed t-test). There was a signifi-cant between-group difference (p< .01), reflectingthe better performance of the subjects whoselesions did not involve the hot spot (mean = 82.2,SD =16.5), compared to the subjects whose lesionsdid involve the hot spot (mean =59.4, SD =26.2).Also, we conducted a Fisher’s exact test on the 54-left-hemisphere subjects who either did or did nothave impaired action naming, and who either did ordid not have lesions that overlapped the hot spot(10/14 subjects whose lesions overlapped the hotspot had impaired action naming, and 31/40 sub-jects whose lesions did not overlap the hot spot hadunimpaired action naming). The result was signifi-cant (p< .005). These outcomes are consistent withthe notion that structures in the hot spot play animportant role in naming actions.

Testing hypothesis 2

With regard to the second hypothesis, it will berecalled that there were two specific predictions.First, we predicted that lesions in regions found tobe associated with impaired action naming wouldspare naming of concrete entities. The results pre-

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sented in connection with the testing of hypothesis1 indicate a “hot spot” for action naming, and asnoted, there were 10 left-hemisphere subjects withimpaired action naming whose lesions overlappedthe hot spot (mean z-score = –8.7). For these 10subjects, the mean z-scores for concrete entitynaming were also in the impaired range (faces, –4.8;animals, –11.2, tools, –9.4). These findings are notconsistent with the prediction, and indicate thatlesions associated with impaired action namingmay also cause naming deficits for concrete entities.

The second prediction was that anterior tempo-ral/inferotemporal lesions (which are associatedwith impaired naming of concrete entities) wouldnot impair naming of actions. The findings sup-ported this prediction. In the 12 subjects in whomthe lesion was completely restricted to the left tem-poral lobe, performance on the Action Naming testwas entirely normal (mean =88.7, SD =4.5), and nosubject in this group was impaired (according to thecriteria depicted in Plate 1). By contrast, all of thesesubjects had naming deficits for concrete entities.These findings support the conclusion that the leftanterior temporal and inferotemporal regions arenot important for action naming, consistent withprevious results regarding this issue (A.R. Damasio& Tranel, 1993; Tranel et al., 1997b).

Follow-up analyses

Action naming versus concrete entity namingTaken together, the results provide only partial sup-port for the second hypothesis, i.e., that there is seg-regation of the neural systems subserving naming ofactions and naming of concrete entities. To explorethis issue further, we calculated a composite con-crete entity naming score for each of the 19 subjectswith left-hemisphere lesions and impaired actionnaming, by averaging the z-scores for the three con-crete entity categories. This composite was thencontrasted with the action naming z-score. Therewere 13 subjects in whom the subtraction of theconcrete entity naming composite z-score from theaction naming z-score was less than –0.5, indicatinga disproportionate impairment in naming actions.Analysis of the lesion overlaps for this group of 13subjects revealed three regions of maximal overlap

(Plate 4, situated between pp. 656 and 657): (1) theleft frontal operculum, underlying white matter,and anterior insula; (2) the left mesial occipital cor-tex; and (3) the paraventricular white matter under-neath the supramarginal gyrus and posteriortemporal region. Furthermore, we observed that ofthe 9 left-hemisphere subjects who had impairedaction naming and whose lesions did not overlapthe “hot spot” identified earlier (cf., Plate 3), 8 werein the group of 13 subjects who had disproportion-ate action naming deficits. Inspection of the indi-vidual lesions of these eight subjects revealed that,in fact, these subjects contributed to the lesion over-laps in the left mesial occipital cortex and in theparaventricular white matter underneath thesupramarginal gyrus and posterior temporal region(the one other subject, who had impaired actionnaming but not disproportionately so, had a leftmesial occipital lesion that overlaps with the areadescribed in part 2 of Plate 4).

Word retrieval versus conceptual knowledgeretrievalAn important issue raised by work on category-related defects concerns the conditions underwhich the defect appears. When a subject fails toretrieve the correct word for a given stimulus (e.g.,an action, or an object), the subject may have intactconceptual (semantic) knowledge of the item, butbe unable to retrieve the pertinent word; or the sub-ject may not have intact conceptual knowledge (ormay not be able to retrieve that knowledge) and, as aconsequence, be unable to retrieve the pertinentword (for more complete discussions of this issue,see Caramazza & Shelton, 1998; H. Damasio et al.,1996; Gainotti et al., 1995; Pulvermuller, 1999;Tranel & Damasio, 1999; Tranel et al., 1997b,1998). In the latter condition, the word-retrievalfailure may be due wholly or in part to a semanticretrieval defect, since a subject cannot be expectedto name an item that is not recognised properly. Inthe first condition, the word-retrieval defect may bepure or mostly so.

Although the current study was not aimed atinvestigating retrieval of conceptual knowledge perse, it is important to establish the extent to whichthe word retrieval deficits noted in our subjects may



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be explained by defects in conceptual knowledgeretrieval. In the case of concrete entities, this issue isdealt with explicitly in the scoring of the items (forcomplete discussions of this topic, see H. Damasioet al., 1996; Tranel et al., 1997b, 1998). Briefly, foreach subject, the naming scores in the categories offaces, animals, and tools are based only on thoseitems for which the subject has produced accuraterecognition. For example, if a subject did not recog-nise (produce accurate conceptual knowledge for) aparticular face or animal, then that item wasexcluded from the scoring of naming success. Inshort, naming scores for concrete entities werebased on items for which subjects had intact, ormostly intact, conceptual knowledge, which meansthe naming scores are relatively pure measures ofword retrieval.

In the case of actions, we pursued this issue byadministering the Picture Attribute Test to the 19left hemisphere subjects with defective action nam-ing. The Picture Attribute Test requires retrieval ofconceptual knowledge for actions (“recognition”),but not naming per se (see Fiez & Tranel, 1997, fora detailed description of the test, and Kemmererand Tranel, 2000a, and Kemmerer, Tranel, andBarrash, 2001, for a further analysis of the process-ing requirements of the test). Briefly, the testrequires subjects to view pairs of pictures depictingdifferent actions, and to choose from each pair thepicture that best meets certain criteria (e.g., Whichaction would make the loudest sound? Whichaction would be most physically tiring?). Scoringwas based on the normative data published by Fiezand Tranel (1997). Each of the 19 subjects withdefective action naming and a left-hemispherelesion was assigned a z-score for the Picture Attrib-ute Test, which represents the number of standarddeviation units that the subject’s score deviatedfrom the mean of normal control subjects.

For each of the 19 subjects, action naming andaction recognition were contrasted by subtractingthe z-score for the Action Naming Test from the z-score for the Picture Attribute Test. In this proce-dure, positive values indicate a greater impairmentin action naming, and higher values indicate a rela-tively greater discrepancy in this direction (i.e.,more impaired action naming, as compared to

action recognition). Across the 19 subjects, theaverage discrepancy of z-scores in this contrast was4.81 (SD =3.4), indicating that on average, the sub-jects’ action naming scores were nearly 5 SDs worsethan their action recognition scores. For the ActionNaming Test, the average z-score in the group of19 subjects was –6.55 (SD = 3.89), whereas theaverage z-score for the Picture Attribute Test was–1.74 (SD =1.61). These scores were significantlydifferent when contrasted statistically with a t-test(p < .001), reflecting the greater impairment foraction naming compared to action recognition.Also, it can be noted that the average z-score for thePicture Attribute Test is above the –2.0 cutoff typi-cally used to classify subjects as “defective”; that is,as a group, the 19 subjects performed within 2 SDsof control subjects in action recognition. Finally,turning to an analysis of individual subjects, it wasfound that only 1 of the 19 had action naming andaction recognition scores that were relatively close(less that 0.5 SDs apart); in all the others, the mag-nitude of discrepancy was 1.1 SDs or greater. In allbut 4 of the 19 subjects, in fact, the discrepancyfavouring action recognition (i.e., a relatively supe-rior performance for action recognition, comparedto action naming) was 2.7 SDs or greater.

Our findings do not guarantee that subjectswhose action naming was impaired had entirelyintact conceptual knowledge and intact access tothat knowledge for all the items that were notnamed correctly. Nor have we ruled out the possi-bility that some of the subjects have deficits at thelevel of semantic knowledge retrieval, especially“lexical” semantics, that would still be compatiblewith accurate performance on the action recogni-tion test described earlier. Complete resolution ofthese issues will require further experimentationwith tasks designed specifically to address suchquestions. In the case of the current findings,though, we consider it unlikely that it would turnout that all of the subjects with impaired actionnaming would be shown to have impairments at thesemantic level, or at the conceptual level, that couldexplain fully their naming deficits. It seems reason-able to suggest, then, that the action namingimpairments identified in our study may reflect, atleast in part, impairments of word retrieval.

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Reclassification of phonological errorsGiven the finding that damage to the frontaloperculum and its vicinity was common in subjectswho manifested impairments of action naming, it isnatural to raise the question as to whether phono-logical errors may have contributed substantially tothe impaired performances of such subjects. Toexamine this question, we conducted a follow-upscoring analysis, focusing on the response errors ofthe 19 subjects with defective action naming andleft-hemisphere lesions. Specifically, we analysedthe proportion of errors that were scored as phono-logical errors, using the specific criteria set forth inKemmerer and Tranel (2000b; see Appendix ofthat paper).

For the overall group of 19 subjects, the averagenumber of such errors was 1.7 (SD = 2.3). Therewere 4 subjects who produced 3 or more phonologi-cal response errors; in the remaining 15, this errortype occurred for 2 or fewer responses. We rescoredthe response protocols of the subjects, giving themcredit for phonological errors. In none of the 19subjects did the rescoring change the subject’soverall classification as having impaired actionnaming. The average z-score for the group of sub-jects, after giving them credit for phonologicalerrors, was –6.3. This is nearly the same as the aver-age z-score of –6.55 obtained when the phonologi-cal errors were scored as errors (as noted earlier),suggesting that this error type contributed verylittle to the action naming deficits of the subjects.

DISCUSSION

We found that the region of highest lesion overlapin subjects with impaired naming of actions encom-passed the left frontal operculum (pars triangularisand opercularis), the inferior sector of the leftprecentral gyrus, the underlying white matter, andthe anterior insula. We also found that lesions inthe left anterior temporal and inferotemporalregions, which produce naming impairments forconcrete entities, did not impair action naming.However, the strong forms of our hypothesesregarding the neural basis of action naming, andregarding the segregation of action naming and

concrete entity naming, were not supported by thefindings, and require qualification. Specifically, wefound that a number of subjects with left premotor/prefrontal lesions and impaired action naming alsohad impaired naming of concrete entities. Also,disproportionate action naming deficits were asso-ciated with lesions of the left mesial occipital cortex,and of the paraventricular white matter underneaththe supramarginal gyrus and posterior temporalregion, in addition to the frontal opercular region.

Our hypothesis 1 proposed that in the case ofactions, some circuits in the left premotor/prefrontal region, in principle separable from theimplementation circuits, operate in a mediationalfashion. Our results suggest that such mediationalcircuits may indeed exist in the region, but it is notpossible, at this point, to separate them anatomi-cally from the implementation circuits. It may bethat with a different method and with differentexperiments, such a separation would be possible(cf., H. Damasio et al., in press); or it may be thatthe mediational and implementation systems are soanatomically close (perhaps even superimposed)that such a separation is not possible. This wouldexplain why some subjects have defects for bothaction naming and concrete entity naming, even ifthe magnitude of those defects differs. The fact thatsome subjects do not have defects for both, how-ever, suggests that there may be a part of thepremotor/prefrontal region that is preferentiallyused as an action naming intermediary system.

The unpredicted anatomical sites identified byour findings suggest that other regions also have animportant role in action naming, namely, those inthe mesial occipital cortex and paraventricularwhite matter underneath the supramarginal gyrusand posterior temporal region. These latter find-ings should be considered in light of the taskdemands of the experiment, which probably requirea considerable degree of mental visualisation of theaction that is implied in the stimulus (Freyd, 1987).The identified sites are critical for the generationand display of visual imagery (Senior et al., 2000;Wheeler, Petersen, & Buckner, 2000). Finally, asfar as the left temporal lobe is concerned, our resultsdo support the segregation of neural systems forconcrete entity naming versus action naming.



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Both the evolutionary and the individual learn-ing factors driving the neuroanatomical placementof the mediational sites related to actions concern:(1) movements of the body and body parts of theagent; (2) characteristic motions of objects; (3) rela-tionships in spacetime; and (4) conditions andchanges of state. By contrast, the equivalent factorsdriving the placement of intermediary regions forretrieval of words for many categories of concreteentities (e.g., persons, animals) concern issues suchas physical characteristics and level of specificity(uniqueness—e.g., my horse “Hawk” versus anonunique, unfamiliar horse) (A.R. Damasio &Damasio, 1994; A.R. Damasio & Tranel, 1993; H.Damasio et al., 1996; Tranel et al., 1997c). Otherauthors have adopted ideas on these issues whoseessence is comparable to ours (Bird, Howard, &Franklin, 2000; Caramazza & Shelton, 1998;Chatterjee, Southwood, & Basilico, 1999; Dixon,Bub, & Arguin, 1997; Goodglass, Wingfield, &Ward, 1997; Gordon, 1997; Humphreys et al.,1997; Kurbat, Smith, & Medin, 1994; Martin,Wiggs, Ungerleider, & Haxby, 1996; Medin,Wattenmaker, & Hampson, 1987; Small, Hart,Nguyen, & Gordon, 1995).

The neuroanatomical proximity of mediationaland implementation structures relative to actionnaming is in notable contrast with the neuroana-tomical separation between mediational and imple-mentation structures relative to concrete entitynaming (see H. Damasio et al., 1996). We suspectthis contrast is due to a primary evolutionary sepa-ration between neuroanatomical structures relatedto the processing of concrete entities, on the onehand, and actions and relationships, on the other.The systems related to actions and relationships arelinked to general spatial processing and movement,and as far as the cerebral cortex is concerned, arelikely to be phylogenetically older and preponder-antly based on dorsal parietal and frontal regions.The preponderance would apply to the structuressubserving conceptual knowledge but would theninfluence structures subserving language. Percep-tual knowledge (and related linguistic knowledge)concerning concrete entities depends somewhatmore importantly, though not exclusively, on corti-ces that can map physical features of entities and

which are predominantly located in ventraloccipitotemporal cortices. We suspect that the par-tial separation that obtains for structures support-ing conceptual and word-form knowledge is moremarked for concrete entities than for actions,largely for the same evolutionary reasons that applyto the distinction between implementation andmediation structures for these same two broad con-ceptual realms.

Our findings should be placed in the context ofrelated functional imaging studies, especially thosethat used a task of generating words for actionsknown as the “verb generate” procedure (althoughthat task and ours have some important differ-ences). Petersen, Fox, Posner, Mintun, and Raichle(1988) found that the generation of an action wordin response to a visually presented word denoting aconcrete entity (e.g., generate “eat” for the word“apple”) produced activation in the left inferiorfrontal gyrus, when compared to a task requiringthe mere reading of the same words aloud (see alsoRaichle et al., 1994). These results have been repli-cated by others (Bartenstein et al., 1994; Grabowskiet al., 1996; Hinke et al., 1993; Wise et al., 1991),and corroborated by lesion-based work (Thomp-son-Schill et al., 1998). Other functional imagingstudies, some of which involved versions of the“verb generate” task (and not all of which involvedovert production of speech), have revealed activa-tion of the left inferior frontal gyrus, in roughly thesame area reported in the Petersen et al. study(Buckner, Raichle, & Petersen, 1995; Demb et al.,1995; Demonet et al., 1992; Frith, Friston, Liddle,& Frackowiak, 1991; Klein, Milner, Zatorre,Zhao, & Nikelski, 1999; Martin, Haxby, Lalonde,Wiggs, & Ungerleider, 1995; Zatorre et al., 1992).Also relevant is a study that revealed activation inthe premotor area when subjects imagined handmovements (Decety et al., 1994). Our currentresults are generally consonant with the gist of thesefunctional imaging studies.

In sum, the evidence from the literature andfrom this study suggests the existence of multiplefunctional systems operating in the left hemisphereto support knowledge retrieval. The systems havesome separable neuroanatomical components, seg-regated by both evolutionary as well as individual

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learning selections. Nonetheless, some compo-nents may be shared or be so anatomically close asto make experimental separation difficult or impos-sible. Moreover, the momentary on-line recruit-ment of system components will vary with differenttask demands, suggesting the existence of “flexible-route” or “preferred-system” arrangements ratherthan rigid paths. The evidence available so far sug-gests that there is a preferred system involving ven-tral occipitotemporal and anterolateral temporalcortices, that excels at processing knowledge forconcrete entities. This ventral system processesfeatural information (e.g., shape, colour, texture)that is critical for the neural encoding of concreteentities, and in its anterior extent, processes the lin-guistic knowledge pertinent to those concrete enti-ties. A second preferred system, comprisingnetworks in the dorsal component of temporo-occipital and parietal cortices and the ventrolateralpremotor/prefrontal region, excels at processingconcepts of actions and their corresponding words.

Manuscript received 27 July 2000Revised manuscript received 18 December 2000

Revised manuscript accepted 5 March 2001

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TRANEL ET AL.


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Plate 1. Distribution of subjects’ scores on the Action Naming Test, plotted according to a least-squares method (bottom) or according tonumber of SDs from the mean of normal controls (top). Bottom: A plot of the raw score (y-axis) versus the score that would be expected werethe data normally distributed (x-axis). This plot shows a clear separation into two approximately normally distributed populations: subjectswith impaired naming scores (red) and subjects with unimpaired naming scores (blue). Each population is fit well by a least-squaresregression (lines), which was used to determine the precise extent of each population (see Methods for additional details). Top: Histogram ofsubjects’ scores, in SDs from the normal mean. The colours refer to the same two populations of subjects depicted in the least-squares graph atthe bottom (red = impaired; blue = unimpaired); darker shades encode subjects with left hemisphere lesions, and lighter shades encode subjectswith right hemisphere lesions.

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Plate2.

Thesubtraction

oflesionoverlapsfor22

unimpaired

subjectsfromthelesion

overlapsfor22im

pairedsubjects,derived

fromM

AP-3

(seetextform

ethods).Thissubtraction

image

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specifictothe

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inthe

figure.

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