Neurocase (2002) Vol. 8, pp. 88–99 © Oxford University Press 2002

Action Sequencing Deficit Following Frontal Lobe Lesion

Sergio Zanini1, Raffaella I. Rumiati1 and Tim Shallice1,2

1Programme in Neuroscience, Scuola Internazionale Superiore di Studi Avanzati, Trieste, Italy and 2Institute of CognitiveNeuroscience, University College London, London, UK

Abstract

Frontal lobe patients carried out temporal sequencing tasks related to actions that differed in terms of theirabstractness using both verbal and pictorial presentations. A generalized impairment was found: neither a type ofaction effect nor a modality of item presentation effect was present. The patients also carried out a correspondingaction production task and produced actions quickly and without errors. The frontal lobe patients were also spared ingenerating verbal descriptions of actions: they were as accurate as normal controls both in terms of the detailsreported and in maintaining the temporal sequence. It has been argued that the difficulty in processing the temporaldimensions of actions following frontal lobe lesions is due to some form of disruption of the action representation.However, no action representational deficits were present in our frontal lobe patients. Thus, they cannot account for ourfindings. On the contrary, we suggest that the action sequencing deficit was a consequence of the difficulties patientsexperienced in rejecting wrong alternatives presented by the stimulus situation.

Introduction

One can consider the organization of human actions on avariety of levels. Schmidt (1975) and Arbib (1985) haveargued that individual subcomponents of a larger skill unitcan be treated as ‘motor response schemas’ formed byabstractions over movements. So during prehension therewould be such schemas for ‘reaching’, ‘pre-shaping’, ‘enclos-ing’ and so on. At a much higher level are scripts (Schankand Abelson, 1977) and the memory organization packets(MOPs) of Schank (1982). They are held to represent thesequence of higher-level operations involved in a familiaractivity like ‘going to a restaurant’ or ‘going to the doctor’.

Between the two in level are activities such as ‘making acup of coffee’, ‘brushing one’s teeth’, ‘starting a car’, wherethe individual subactions appear to be controlled by discreteoperations such as ‘stir the coffee’ (in making a cup ofcoffee) which are in turn themselves very close to the lowest-level motor response schemas. This third domain, which wecall lower-level schemas (or schema-type actions), is that ofsimpler actions where each single step is typically carriedout in a highly specific manner in order to reach the actiongoal. Normally when one prepares orange juice, say, theorange is cut in one particular manner, namely by sawingthe orange and not by pushing down the knife as is done whenone is cutting butter. By contrast, higher-level representationssuch as scripts or MOPs do not necessarily relate directly toeffector systems. Thus, the step of ‘paying the bill’ in the‘going to the restaurant’ script may be realized by making

Correspondence to: S. Zanini, Cognitive Neuroscience Sector, SISSA, Via Beirut 2–4, 34014 Trieste, Italy. E-mail: zanini@sissa.it or T. Shallice, Institute ofCognitive Neuroscience, University College London, Alexandra House, 17 Queen Square, London WC1N 3AR, UK. E-mail: t.shallice@ucl.ac.uk

out a cheque, counting out notes or signing a credit cardslip. Moreover, at this higher level, operations are typicallyinterleaved by many other activities such as visiting a shopwhen going to the doctor. This can also happen when brushingone’s teeth, say, but it is unusual and often counterproductive.Thus, the lower-level schemas and higher-level scripts differon a number of dimensions [see Cooper and Shallice (2000)for a discussion].

Frontal patients have been reported to experience impair-ments in action processing at both the schema and the scriptlevels. In particular, after Luria’s (1966) pioneering studies,several single-case studies have been carried out by Schwartzet al. (1991, 1995, 1998) and by Humphreys and Forde(1998), where attention has been mainly directed to deficitsin the production of actions of the schema type followingextensive lesions involving the frontal lobe.

In this paper, we will, however, focus our attention on asecond group of investigations (Sirigu et al., 1995, 1996,1998; Partiot et al., 1996; Crozier et al., 1999) which haveconsistently shown the pre-frontal cortex to be involved at ahigher level of cognitive control in the processing of thetemporal structure of script actions. Sirigu et al. (1995)compared pre-frontal patients with posterior patients andnormal controls. Several striking findings were reported. Ina script generation task—the evoking of as many actionsteps as subjects could think of—the three groups reportedapproximately the same number of script steps and followed

Action sequencing deficit 89

the intrinsic temporal order of the action. However, only thepre-frontal patients made early closures of the scripts andmade sequence errors which violated the temporal structureof the scripts. Moreover, the pre-frontal patients producedmore errors in sequencing novel and non-routine scriptscompared with routine ones.

Sirigu et al. interpreted these data in the light of Grafman’s(1989) theory of managerial knowledge units (MKUs) whichare defined as ‘single units of memory representing thematicand temporal aspects of event series...’ (Grafman, 1994).MKUs can be considered closely related concepts to scriptsand MOPs. Pre-frontal patients evoked as many script stepsas posterior patients and normal controls. Thus, basic repres-entation of the scripts was held to be stored in other corticalareas in association with lexical and semantic information.By contrast, lesions to pre-frontal cortex were suggestedto damage aspects of scripts such as temporal sequence,boundaries and priority sets, which the authors labelled asaspects of the script ‘grammar’ for logical and temporal order.

Two comments can be made. First, it is argued that thebasic representation of the script is spared after pre-frontaldamage, but that the MKUs are not. The theory claims thatthe MKU is characterized by a functional network thatassembles basic script information into the correct temporalsyntax. In order to corroborate this theory, it would beimportant to verify the independence of the MKU from basicknowledge by comparing pre-frontal patients with posteriorones having basic semantic knowledge deficits, e.g. insemantic dementia. In fact, the posterior group, in this study,did not differ from the normal controls. No one has yetreported the contrasting dissociation of a disorder of script‘grammar’, due to a pre-frontal lesion, compared with a‘semantic’ deficit due to a posterior lesion.

The second comment concerns the claim that these findingsprovide some support for MKU theory. Subjects had to givethe steps involved in three situations: going to work, planninga trip to Mexico and starting up a beauty salon business.Only the first would qualify as just a script. The second andparticularly the third contain major problem-solving elements,and these may be the cause of any frontal impairment,particularly in the generation task.

In a following paper, Sirigu et al. (1996) investigated thesame patients reported in Sirigu et al. (1995) on both scriptsequencing and script sorting tasks. They replicated theearlier findings on sequencing and also found a selectiveimpairment in boundary maintenance of scripts in the pre-frontal population. The patients tended to mix scripts together,to fuse them, and to include distracters into legitimate scriptsor to create new implausible scripts with distracters only.The authors interpreted these findings by slightly modifyingtheir previous (Sirigu et al., 1995) theoretical position.They suggested that sequence information for scripts can beencoded in two ways: the first by posterior cortex associativenetworks that store the coarse temporal contiguity betweenan initial state, an action and a final state, as well as semanticassociations between script elements; the second by a frontal

network that can store any sequential patterns of activation.Thus, they claimed that the pre-frontal cortex ‘stores anarbitrary sequence using the consequence of the action as abinding agent between context and action, instead of atemporal correlation’ (Sirigu et al., 1996, p. 308). Therefore,the authors suggested that the finer temporal structure ofscripts is automatically shaped when pre-frontal areas triggerscript element activation in a top-down manner. In theauthors’ view, this theory could account for frontal patients’script processing performances characterized by the mainten-ance of a general chronological organization of scripts (dueto intact posterior cortex representation), interrupted byfrequent steps back in time (due to loss of more fine-grainedpre-frontally stored information). This interpretation was notspecifically supported by neuropsychological evidence, as noassessment of working memory was carried out.

In a recent paper, Sirigu et al. (1998) carried out furtherinvestigations on the processing of sequences followingfrontal lobe lesions. They compared four Broca’s aphasicswith lesions not involving the pre-frontal cortex and fourpre-frontal patients with lesions not affecting Broca’s area.The Broca’s aphasics were able to sort and sequence actionscripts but failed on a sentence ordering task. The pre-frontalpatients were able to sequence parts of sentences correctly,respecting given syntactic cues, and to sort scripts but wereimpaired in ordering script elements. This double dissociationbetween sentence syntax and story grammar sequencingwas interpreted as resulting from the independence of theunderlying cognitive processes. The process of ordering,typically attributed to frontal lobes, was believed to bespecific to the type of item to be ordered. These authorsclaimed that it is unlikely that ordering depends ‘on asupramodal processor, but [it] is rather a function of the typeof underlying knowledge structure to be processed’ (Siriguet al., 1998, p. 776).

Two neuroimaging studies addressed script processing innormal subjects (Partiot et al., 1996; Crozier et al., 1999).In the Partiot et al. (1996) positron emission tomographystudy, normal subjects were expected to judge whether agiven script step belonged to a certain script (content aspectsof the script) and to judge whether a given script stepoccurred before or after another one (formal temporal aspectsof the script), with a font discrimination task as the baselinecondition. They found activations of the right frontal lobe,the left superior temporal gyrus and the middle temporalgyrus bilaterally during the first task. In contrast, the leftfrontal lobe, the left anterior cingulate and the anterior partof the left superior temporal gyrus were more active duringthe second task. The authors concluded that temporal orderingof scripts and determining whether an event belongs to aparticular script seem to be processed by distinctive neuronalnetworks.

In the Crozier et al. (1999) functional magnetic resonanceimaging study, the authors tried to confirm Sirigu et al.’s(1998) findings. They reported a major activation of rightand left middle frontal gyri, the left supplementary motor

90 S. Zanini, R. I. Rumiati and T. Shallice

area and the left angular gyrus in a script sequencing taskcompared with a sentence sequencing task. They interpretedthis finding by claiming that the regions activated in thiscondition contain neural circuits involved in action planningand specifically in their temporal ordering when representa-tions from long-term memory are recalled. They made thehighly speculative suggestion that these areas are recruitedwhen an event sequence representation is activated, in analogyto Bottini et al.’s (1994) evidence of right middle frontalactivation during metaphor plausibility judgement tasks.

In fact, the study failed to show a clear-cut doubledissociation. By contrast to the several areas that weremore activated during script processing, no areas weremore active during the syntactic task. Therefore, thefindings basically corroborate a pre-frontal involvement inscript processing.

As can be seen, Sirigu et al. have provided extensiveevidence that the frontal lobes are heavily involved inprocessing the temporal structure of scripts. However, thetheoretical accounts provided are very speculative. No strongevidence has been obtained for either the script syntaxrepresentation or the working memory hypotheses. In addi-tion, these group studies on temporal processing of actionsin frontal lobe patients have concentrated on one type ofaction only (i.e. script-level actions) and one type of modalityonly (verbal presentation of stimuli) (Sirigu et al., 1995,1996, 1998).

Therefore, the present study had the following aims:(1) to assess, by analogy with Sirigu et al.’s studies, whether

the ordering of different levels of actions, namely onepertaining to the schema level (Schimdt, 1975; Normanand Shallice, 1986; Cooper and Shallice, 2000) and moreabstract ones pertaining to the script level (Schank andAbelson, 1977) are processed differently in frontal lobepatients and to assess whether different modalities ofitem presentation (verbal and pictorial) have an effect onaccess to action knowledge;

(2) to assess whether the subcomponents of action could beeffectively ordered in other types of task;

(3) to assess whether action sequencing impairments correl-ate with more basic sequencing deficits in frontal lobepatients.

Subjects

Nine consecutive right-handed patients with cerebral lesionsinvolving frontal lobes (in three cases the lesion extended tothe temporal lobe) (Fig. 1) were tested. A set of baselineneuropsychological tests was administered to assess generalintelligence, language functions, attention, praxis abilities,executive functions, memory and visuospatial abilities (seeTable 1). Nine age-matched normal controls [mean age 60.11years, standard deviation (SD) 12.11] were compared withthe frontal lobe patients.

Section 1. Action sequencing

Experiment 1 (conditions a, b, c, d)

Four different action sequencing tasks were given to theexperimental subjects. Two sets of schema-type actions (e.g.‘preparing orange juice’) (experiments 1a and 1b) and two setsof script-type actions (e.g. ‘having a meal at the restaurant’)(experiments 1c and 1d) were used. Each had to be carriedout in two different conditions, using pictures (experiments1a and 1c) and verbal descriptions (experiments 1b and 1d).Ten schema-type actions and 10 script-type actions wereused (see Appendices 1 and 2).

The selected actions were highly familiar to all patients.Only salient action steps—steps belonging to what we willcall an ‘ordinate’ level (Schank and Abelson, 1977)—wereincluded in the sequence (e.g. for schemas—‘opening a tinof tuna fish’: holding the tin opener, cutting the lid, bendingback the lid, lifting the tuna on to a plate with a fork; forscripts—‘going to the doctor’: sitting in the waiting room,entering the doctor’s office, undressing, lying on the bed,dressing, leaving the doctor’s office). The same steps werepresented in the verbal and pictorial modalities. We askedseven normal subjects, not involved in the study, to checkwhether the action sequences included subordinate- ratherthan ordinate-level steps (e.g. in the script ‘going to thedoctor’, the step ‘undressing’ might be described also includ-ing subordinate actions such as ‘unbuttoning the shirt’ or‘taking shoes off’). They all agreed that the sequences didnot do so. Using this criterion, the schema sequences rangedfrom four to six steps while the script sequences ranged fromfive to eight steps. A complete balancing of action sequencelengths between schemas and scripts was not possible due tothe different ranges of sequence lengths that naturally occur.

Cards, each representing a single action step, were placedin a pseudo-random order on the table in front of the subject.All the cards had to be changed to obtain the correct solution.All subjects were given the same order for any given set ofstimuli. No time limits were imposed. They were allowed torearrange the cards as many times as they wished. To bescored correct, the sequence had to be eventually correct.The patients were tested in the four experimental conditionsin four separate testing sessions.

Results

The patient group scored far below the control mean on allaction sequencing tasks (see Fig. 2). In experiment 1a(schema–pictorial) their mean score on all correct sequencerearrangements was 33.3% (SD � 23.4), highly significantlyless than the normal mean of 95.6% (SD � 7.3) (t � –7.91,P � 0.0001). In experiment 1b (schema–verbal), the patientsrearranged 37.8% (SD � 28.6) sequences correctly while thenormal controls scored 90% (SD � 13.2) correct, highlysignificantly more (t � –4.76, P � 0.0001). In experiment1c (script–pictorial), the frontal lobe group again had apathological performance: their mean score of 23.3%

Action sequencing deficit 91

Fig. 1. Lesion diagrams of each of the nine patients (right and left sides are inverted such as in computed tomography scans).

(SD � 28.7) was significantly less than the normal mean of80% correct (SD � 22.3) (t � –4.54, P � 0.0001). Inexperiment 1d (script–verbal), the patients scored 24.4%correct (SD � 27.9), significantly worse than the control

subjects who scored 96.7% (SD � 5) correct (t � –7.4,P � 0.0001).

An inter-test correlation analysis revealed that the script–pictorial and schema–pictorial tests correlated highly with

92 S. Zanini, R. I. Rumiati and T. Shallice

Table 1. Neuropsychological assessment

Patient

1 2 3 4 5 6 7 8 9

Age (years) 75 48 74 38 75 64 27 64 59Lesion site LF LF LF(T) BF LF(T) RF BF BF BF(T)

Brodmann areas 6,44,45,46 6,24,45 6,9,22,41, 8,9,10, 6,9,10, 8,9,10,24, 4,6,24,32 9,10,12, 6,9,10,11,42,44,45,47 24,32,45,46 22,44,45,46 32,44,45,46 24,32,44, 12,21,22,24,

45,46 31,38,45,46Aetiology Vascular Vascular Vascular Traumatic Vascular Vascular Traumatic Traumatic VascularIntelligence

WAIS IQ 86 92 95 93 87 66 76 86 86Language

AAT Broca Broca Broca Not aphasic Broca Anomic Anomic Not aphasic Not aphasicAttention

Attention matricese 28/60 35/60a 20/60a 48/60 29/60 17/60a 57/60 44/60 44/60Praxis

Ideomotor apraxia 41/72b 60/72 44/72b 68/72 61/72 38/72b 64/72 61/72 62/72Ideational apraxia 14/14 14/14 14/14 14/14 14/14 14/14 14/14 14/14 14/14Buccofacial apraxia 10/20a 15/20a 11/20a 19/20a 14/20a 18/20a 17/20a 20/20 17/20a

Constructional apraxia 6/14a 12/14 9/14a 10/14a 3/14a 2/14a 10/14a 9/14a 14/14Executive functions

Weigl (No. categories) 1b 1b 1b 2 2 1b 2 1b 1b

WCST(No. categories) 1a 2a 1a 2a 2a 1a 2a 1a 1a

Perserverative errors (%) 48c 61c 32 63c 76c 77c 32 79c 100c

Brixton (scaled score) nt nt nt 3 1 1 nt 1 2Reversed digit span nt nt nt 3a nt 2a 5 3a 2a

MemoryDigit span 9/24d 6/24d 11/24d 6 11/24d 4a 5 5 6Story recall nt nt nt 3.3/16a 6.6/16 3/16a 11.6/16 4.2/16a 5.3/16a

Corsi test 2a 5 4 5 4 4 6 4 4Visuospatial ability

VOSP screening 20/20 16/20a 20/20 20/20 16/20a 20/20 20/20 20/20 20/20VOSP object decision 17/20 17/20 15/20 16/20a 11/20a 11/20a 19/20 16/20 17/20BORB (T8) 21/25 23/25 22/25 24/25 21/25 18/25 24/25 22/25 24/25BORB (T12) 25/30 27/30 30/30 29/30 26/30 21/30a 26/30 26/30 30/30

aPerformance falling 1.5 or more standard deviations below normal mean.bPerformance falling below cut-off.cPerformance falling above the pathological cut-off.dProbe recognition (six words version).eSpinnler and Tognoni, 1987.L, left; R, right; B, bilateral; F, frontal; T, temporal; nt, not tested; WAIS, Wechsler Adult Intelligence Scale; AAT, Aachen Aphasia Test; VOSP, Visual Objectand Space Perception battery; BORB (T8), Birmingham Object Recognition Battery foreshortened match; BORB (T12), association match test; WCST, WisconsinCard Sorting Test.

each other (Spearman’s rho � –0.76, P � 0.02), as didthe script–verbal and schema–verbal tests (Spearman’srho � –0.78, P � 0.02). The script–pictorial test sequencingtest correlated (Spearman’s rho � –0.69, P � 0.04) withthe buccofacial apraxia test, as did the script–verbal(Spearman’s rho � –0.76, P � 0.02) and the schema–verbal tests (Spearman’s rho � –0.79, P � 0.02). Onepossibility is that these correlations come from anatomicalcontiguity. The other significant correlation of the sequen-cing tests with a neuropsychological baseline test was thescript–pictorial test with the Corsi block test (Spearman’srho � –0.68, P � 0.04). The correlations of the Corsiblock test with the other three sequencing tasks were farfrom significant (all P � 0.2).

We further analysed the performances of the patients andcontrols in order to reveal whether there was an action-typeor modality-type effect, namely whether they differed in

sequencing actions of different types or actions presentedwith different stimuli. An ANOVA for repeated measureswith arc-sine transformation of raw data was run to testwhether the subjects’ performances differed in respect to thetype of action (schema versus script) or type of stimulus(verbal versus pictorial). A 2 � 2 � 2 design was set: typeof action (schema versus script) � modality (verbal versuspictorial)�group (frontal patients versus control subjects).The main effect of group was significant: the patients’performance was lower than that of the control subjects(F1,16 � 53.1, P � 0.0001). The main effect of type of actionwas also significant (F1,16 � 9.01, P � 0.01). Overall, thesubjects made more errors in sequencing script actions thanschema actions. No difference between verbal and pictorialpresentation of stimuli was found (F1,16 � 0.53, P � 0.4).No interactions were found.

One possibility is that the effect of type of action could

Action sequencing deficit 93

Table 2. Comparison of schema- and script-type actions controlled for sequence lengths expressed as a percentage of the total

Patients Controls

Schema Script P Schema Script P

Total correct rearrangementsSchema 5 versus script 5 26.8 23.0 ns 92.9 89.8 nsSchema 6 versus script 6 29.7 25.4 ns 94.4 92.0 nsSchema (5�6)/2 versus script (5�6)/2 28.2 24.2 ns 93.5 90.9 ns

Correct placement within action sequenceSchema 5 versus script 5 43.2 42.6 ns 95.8 93.9 nsSchema 6 versus script 6 55.6 52.0 ns 97.2 94.0 nsSchema (5�6)/2 versus script (5�6)/2 49.4 47.3 ns 96.5 94.0 ns

Schema/script 5, schema/script-type actions of five steps; schema/script 6, schema/script-type actions of six steps; schema/script (5�6)/2, averaged score ofschema/script-type actions of five and six steps; ns, not significant.

just be a result of the difference in length of the action stepsequences between the schema and the script stimuli. For theformer stimuli, sequences were of four to six steps whilstfor the latter they ranged from five to eight. Correlationanalyses between the length of action sequences and thenumber of correctly rearranged sequences of that lengthproved significant only in the patient group (Spearman’srho � –0.41, P � 0.01). In order to assess the possibilitythat the overall type of action effect came from the averagelength difference between the groups, we compared theperformance of the patients and the control subjects on schemaversus script actions of the same length. The performances onschema and script actions of five and six steps were compared.In addition, the same comparisons were made on the percent-age of correctly positioned action steps within actionsequences. No significant difference was found for eithercomparison (see Table 2). Thus, the patients and the controlsubjects both had comparable performances for schema andscript sequences when length was controlled. Thus, theperformance of the patients and the control subjects onaction sequencing tasks (experiments 1a, 1b, 1c, 1d) differedbetween schema and script actions simply because the script-type action sequences were overall somewhat longer.

Error analysis

We further analysed action sequences in order to determinewhether there was a particular pattern of error occurrence inthe sequences, contrasting the initial, the central and the laststeps. An ANOVA with a 3 � 2 design was carried out:position (first versus central versus last)�group (frontalpatients versus controls), with data being transformed usingthe arc-sine procedure.

The main effects of position (F2,156 � 26.04, P � 0.0001)and of group (F1,78 � 318.02, P � 0.0001) and the interactionposition�group (F2,156 � 4.2, P � 0.017) were all significant.Overall, the central steps were positioned less correctly thanthe extreme steps (Fig. 3 shows the typical U-shaped curve).Moreover, the control subjects performed better than thepatients. The frontal patients differed in sequencing thecentral steps compared with the extreme steps, while

Fig. 2. Experiment 1. Percentage correct scores of frontal lobe patients andcontrol subjects on action sequencing tasks across different conditions.

Fig. 3. Experiment 1. Percentage of action steps correctly positioned in actionsequencing tasks. Only frontal lobe patients showed a U-shaped curve: centralaction steps were less correctly positioned compared with the extreme stepswithin the action sequence.

the control subjects did not. Post-hoc analyses, using pairedsample t-tests for each comparison with Bonferroni correc-tions for the number of comparisons, revealed that the centralsteps were positioned significantly less correctly comparedwith the extreme steps: (first step versus central step:t39 � –4.96, P � 0.0001; first step versus last step:t39 � –1.41, P � 0.17; central step versus last step:t39 � –5.62, P � 0.0001).

Discussion

Overall, the performance of the patients on the sequencingtasks remained far below that of the controls, revealing ageneralized action sequencing deficit. This behaviourcharacterized the performance of the patients on all action

94 S. Zanini, R. I. Rumiati and T. Shallice

sequencing tasks irrespective of the type of action (schemaversus script) and the modality of item presentation (verbalversus pictorial). Therefore, we confirmed previous findings(Sirigu et al., 1995, 1996, 1998) which involved only verballypresented script sequences, and extended them to pictorialpresentations and to actions belonging to the schema level(Schank and Abelson, 1977). The effects were greater withscript than with schema stimuli, but when sequences of equallength were compared there were no differences.

An analysis of the position at which errors occur wascarried out. When the patients were required to rearrangeaction verbal descriptions or action pictures, they reproducedthe outer portions of the action sequences relatively betterthan the central section. This effect was not found in thecontrol subjects.

Two possible explanations of our findings could be thatthey are due to a disruption of the action representations perse or to a failure in understanding the sequencing tasks.These alternative explanations are assessed in sections 2, 3and 4, respectively.

Section 2. Schema production

Experiment 2

In experiment 2 we asked the subjects to produce 10 routineschema actions which were very familiar to Italian people(the same as in experiment 1). We selected multiple-objectactions as we assumed that they would be a more sensitivetool, compared with single-object use tasks, to unmask anydeficit in action production. Between three and five objectsper action were required for each action to be produced.They were on the table in front of the subjects. No distractingobjects were given. Patients with motor impairments due toweakness were helped by the experimenter, as some hadlimb paresis (e.g. the experimenter held the lower part of thecoffee machine whilst the patient was screwing the upperpart on to it).

No time limits were imposed. The patients were videotapedfor subsequent scoring. Action productions were scored usingan action error taxonomy utilized in a previous study on twoapraxic patients (Rumiati et al., 2002). The following errorswere scored: kinematic errors: clumsiness, namely trajectoryand grasping errors; sequence errors, namely errors occurringat the temporal sequence of the action: (a) action addition,insertion of a meaningful action step that is not necessary toaccomplish the goal of the action, (b) action anticipation,anticipation of an action that would normally be performedlater in the action sequence, (c) step omission, omission ofa step of the multiple action sequence, (d) perseveration,repetition of an action step previously performed in the actionsequence; conceptual errors, namely errors that are concernedwith the conceptual aspects of objects and actions: (a) misuseof the object, the object is used in an inappropriate manner,(b) mislocation of the action, the action is appropriate to theobject but is performed in the wrong place, (c) tool omission,

Fig. 4. Experiment 2. Percentage of schema actions (the same as selected forexperiment 1) correctly produced by frontal lobe patients and control subjects.

omission of an obligatory tool, (d) pantomiming, instead ofusing the object, the patient pantomimes how it should beused, (e) perplexity, delay and hesitation in starting an actionor a subcomponent of an action, (f) toying, brief but repeatedtouching of an object or objects on the table.

The presence of any of these error types in the sequenceof action steps led to it being treated as an action error.

Results and discussion

As a group, the performance of the patients did not differfrom that of the normal control group (patients’ mean %correct actions � 93.3, SD � 10; controls’ mean % correctactions � 95.5, SD � 7.3; t � 0.51, P � 0.6) (see Fig. 4).No deficits in action production were present. In detail, thepatients made three action addition errors, one step omissionerror, two misuse errors and one tool omission error. Thecontrol subjects made two step omission errors and threetool omission errors. These findings are not consistent withthe view of a deficit of any aspect of action representationin the frontal lobe group. A representational deficit wouldlead to an impaired performance in action processing irre-spective of the task (action sequencing versus action produc-tion). Therefore, the action sequencing deficit requires analternative interpretation.

Section 3. Schema and script generation

Experiments 3a and 3b

In experiments 3a and 3b the subjects were asked to producedescriptions (i.e. verbal generation task) of 10 schema actionsand 10 script actions, respectively (the same as those usedin experiment 1). The instruction was as follows: ‘Pleasedescribe to me how the following action is performed, stepby step’. This test could only be administered to six of thenine patients, as three had a severe Broca’s aphasia. Five ofthe patients had normal language production and one (number2) was still able to produce a sufficient amount of languagefor task performance, as assessed by the Aachen AphasiaTest (Luzzatti et al., 1996) in the clinical evaluation.

Results

We submitted the number of action steps generated by thefrontal lobe patients and the control subjects to t-tests in

Action sequencing deficit 95

Fig. 5. Experiment 3a. Absolute number of action steps evoked by frontallobe patients and control subjects during the verbal description of a schemaaction (the same as selected for experiment 1).

Fig. 6. Experiment 3b. Absolute number of action steps evoked by frontallobe patients and control subjects during the verbal description of a scriptaction (the same as selected for experiment 1).

order to evaluate whether the patients produced poorer actiondescriptions verbally. The patients verbally generated thesame number of action steps as the controls. No differencesbetween groups were obtained in the total number of schemaactions (F1,10 � 0.31, P � 0.5) and in the total number ofscript actions (F1,10 � 0.004, P � 0.9). Occasionally thefrontal patients added some irrelevant steps to the core actionsequence. For instance, in the schema action ‘preparingorange juice’, one patient added action steps such as ‘purchas-ing the orange’ or ‘washing hands’ and so on. In order toevaluate this phenomenon, we asked two independent judges,who did not participate in the study, to sort the action stepsreported by the patients and the control subjects into threeclasses: (a) relevant steps (i.e. steps necessary to perform thevery core of the action, i.e. those used in experiment 1);(b) irrelevant but appropriate steps (i.e. action steps that canbe done but do not belong to the very core of the action);(c) irrelevant and inappropriate steps (i.e. action steps thatdo not belong to the action at all). We compared the meannumber of relevant action steps evoked by the patients andthe control subjects using t-tests for schema and scriptactions. No differences were found for the former actiontype (F1,10 � 0.47, P � 0.6) (Fig. 5) or for the latter(F1,10 � 0.40, P � 0.7) (Fig. 6). Only two frontal lobepatients added several (in one case seven and in the othercase six) irrelevant but appropriate action steps, while thecontrol subjects did not. No irrelevant and inappropriateaction steps were added by anyone. Therefore, the results of

experiments 3a and 3b did not depend on the inclusion ofadditional steps to the correct action descriptions.

In addition, unlike their performance on sequencing tasks,the six patients always produced action descriptions in thecorrect temporal order, respecting the action sequences. Forinstance, one patient described the script ‘going to the cinema’as follows: I purchase the ticket, I walk towards the room,I show the ticket, I enter the room, I sit down. By contrast,the rearrangement of the same script for the action sequencingtask carried out previously (experiment 1) was as follows: Ienter the room, I walk towards the room, I sit down, Ipurchase the ticket, I show the ticket. There was a dissociationbetween the performance of the patients on this test and onthe action sequencing test (experiment 1).

This effect was not due to the selection of the patients.The mean percentage score of the six patients tested in theexperiment on the schema sequencing task (experiments 1aand 1b) (mean of pictorial and verbal modality) was 30.1%,while they produced the correct action sequence in 98.3% ofactions, on average, for the schema evocation task. Similarly,they scored 30% on the script sequencing task (experiments1c and 1d) and maintained the appropriate action sequencein 96.7% of actions, on average, on the script evocation task.

Discussion

The patients were able to recall from long-term memory boththe content (i.e. the correct action steps without includingaction steps belonging to other schemas or scripts) and thestructure (i.e. the correct temporal sequence) of the actions.As far as the results with schema stimuli were concerned,this was true irrespective of the required output method:motor production in experiment 2 and verbal generation inexperiments 3a and 3b. These findings suggest that there isno representation deficit for well-learned actions in this groupof frontal lobe patients. However, an alternative interpretationcould be that the action sequencing impairment is due to afailure to understand the task. This will be considered in thenext section.

Section 4. Basic sequencing tasks

Experiment 4 (conditions a, b)

We asked the nine frontal lobe patients and the nine controlsubjects to carry out two other sequencing tasks in order tocheck for the presence of any deficit in understanding thetask. In experiment 4a, 10 sets of five geometric shapes (fivetriangles, five squares, etc.) of different sizes were used. Thesubjects were asked to rearrange the shapes from the smallestto the largest. In experiment 4b, 10 sets of five Arabicnumbers, ranging from 1 to 99, were used. The subjectswere required to sequence the numbers from the lowest tothe highest.

The shapes and the numbers were presented on individualcards and were placed in a pseudo-random manner on the

96 S. Zanini, R. I. Rumiati and T. Shallice

table in both tasks (all the cards had to be moved to carryout the task). No time limits were imposed. The presence ofone or more step errors invalidated the action sequencerearrangement.

Results and discussion

Both the patients and the control subjects were completelycorrect on both tasks. No basic sequencing deficits werefound in the frontal lobe patients. This rules out the possibilitythat the action sequencing impairment found was determinedby a failure to understand the task.

General discussion

We investigated action processing in frontal lobe patients.We submitted the patients to four action sequencing tasksrelated to schema-type actions (Schmidt, 1975) and script-type actions (Schank and Abelson, 1977), presenting eachboth verbally and pictorially. We found a generalized impair-ment in action sequencing. Neither a type of action effectnor a modality of item presentation effect was present. Wealso submitted the patients to two basic sequencing tasks,shape and number sequencing, as Humphreys and Forde(1998) had reported that their individual frontal lobe patientshad some sequencing deficit when letters and numbers wereused. Our patients performed these control tasks perfectly.Therefore, no basic deficit of sequencing comprehensioncould account for the action sequencing impairment.

The action representation deficit

Can the theoretical position tentatively put forward by Siriguet al. (1995) and more definitively by Sirigu et al. (1996,1998) [see also Humphreys and Forde (1998)] give anexplanation of our findings? This view claims that the frontallobes play a critical role in storing at least some aspects ofthe representation of well-learned actions, particularly thoserelating to their temporal organization.

In order to investigate further the action representationdeficit hypothesis, we asked the patients to produce verbaldescriptions of both types of action (schema and script)description. The frontal patients performed as well as thenormal controls on these tasks. Moreover, they respected theappropriate sequence of the subactions. This is difficult tointerpret within an action representation deficit hypothesis.In this case, the patients should not have been able to evokethe details of the action steps or to respect action sequences.These representations would also appear to include the finertemporal action sequence representations, contrary to Siriguet al.’s (1996) claim. In addition, we asked the patients tocarry out schema actions. Their performance was comparablewith the performance of the control subjects. This studysuggests that the action representations were intact given thatthe correct ordering of objects can hardly be carried out byaffordance.

Of course, it could be argued that the script syntaxrepresentations with which Sirigu et al. were concerned relateto MKUs and not to schema-type actions. However, onewould then have to explain why our group of frontal patients,who showed the same general type of problem to theirs onordering script-type actions, also had identical problems inordering schema-type actions. There were no differencesbetween action types when they were directly compared withthe length effect controlled for. In addition, they showed asimilar serial position effect within the action sequences,which was not shown in the normal subjects. Thus, it wouldappear that a set of processes common to temporal orderingin the two tasks was required.

Working memory

In their 1996 paper, Sirigu et al. put forward the workingmemory hypothesis. They suggested that the difficulties thatpre-frontal patients experienced on the sequencing tasks arosefrom a working memory deficit (even if assessment of thiscognitive function was not carried out), which produces adifficulty in maintaining the finer script structure. Their viewis that pre-frontal lesions, sparing the posterior associativecortex where the gross temporal structures of scripts arestored, lead patients to respect only the rough temporalorganization of action. However, if the difficulty arises froma working memory problem, it is unclear why the patientscan actually produce verbal descriptions of the sequenceof actions.

Relationship to other studies

It might seem that there is a discrepancy between our scriptgeneration findings and those of Sirigu et al. (1995). In fact,Sirigu et al. only tested a single routine action and there wasno significant difference between their patient groups onclosure or sequence errors with this single action. Moreover,the finding of analogous effects in the sequencing of schemaand script actions is very different from that of Sirigu et al.(1998) who used sequences of script and sentence material.However, their finding of a double dissociation between twotypes of material only requires that one involves specificsequencing processes different from other sequencing opera-tions (Kinsbourne, 1971; Shallice, 1988). In the Sirigu et al.(1998) case it is most plausible that this is the sentencematerial where performance would be impaired by a specificagrammatism.

Our results on action production differ from those ofHumphreys and Forde (1998) who also studied patients whohad frontal lobe lesions. They reported two patients, FKand HG, who were impaired on action production, actionevocation and action sequencing tasks. This generalizedaction processing deficit was interpreted as an effect ofdisordered action schemas. They proposed that, within aschema, long-term knowledge of actions and the associatedinformation about their temporal order are intimately linked.

Action sequencing deficit 97

In fact, their patients had large lesions that extended outsidethe frontal lobes (notably FK had bilateral temporal lesions)and, indeed, FK was only able to name 41% of the objectsused in the action production tasks—whether this was dueto a pure naming or an agnosic deficit remains unclear.However, it is clear that our patients differed qualitativelyfrom these, possibly due to differences in lesion sites. Thus,our study cannot shed light on the effects they found.

One study which is complementary to the present one inproducing a double dissociation is that of Rumiati et al.(2002) who described two ideational apraxic patients (DRand FG) with left parietal lesions who had impaired perform-ance on an action production task but showed a normalprofile on an action sequencing task. The occurrence of thisdouble dissociation supports the idea that a sequencing deficithas nothing to do with the nature of the underlying actionrepresentations. Rumiati et al. proposed to interpret thesefindings in the light of Norman and Shallice’s (1986) modelof willed actions, recently updated by Cooper and Shallice(2000). The impairment in producing well-learned actionswas held to be due to a disruption within the cognitivesystem devoted to schema storage and action selection,namely the contention scheduling system.

If one looks in more detail at the occurrence of errors inaction sequencing tasks, a major impairment with respect toaction temporal organization in the middle of an actionsequence was found. In this, our findings replicate those ofSirigu et al. (1996) who found that frontal lobe patientsrespected, even if only partially, boundaries (i.e. extremeaction steps) more than the finer temporal structure of scripts.It seems reasonable to assume that defining the borders ofan action sequence requires less resources because thesesteps are more easily recognizable. To select the appropriatesequence of central steps seems likely to make extensivedemands on executive functions. First, it requires the patientsto simulate mentally the whole temporal structure of theaction. Second, for each element of the sequence the patientsmust create a correspondence between the verbal or visualtoken and the internal abstract representation of the action.We presume that the patients are potentially capable ofboth of these steps from the normal performance in verbalgeneration of action descriptions (experiments 3a and 3b).However, this does not mean that the patients necessarilycarry out these steps satisfactorily when the task implicitlyrequires it rather than explicitly demands it of them.

The third and potentially most critical stage involvesthe organization of the operations involved in solving thesequencing problem. This is not a routinized skill for mostsubjects. If, say, the patients consider any two cards at anyone time, then he or she must see whether there is or is nota discrepancy with the ‘real’ ordering. If there is a discrepancy,then the pair must be switched round. Most crucially thisprocess must be repeated not just on the cards as yetunchecked, but also on the cards already switched, as theymay conflict in their new positions with cards other than theones with which they had been compared. To organize the

programme of comparisons, and thus of possible switchingoperations, appropriately would require a novel strategy formost subjects. A more basic process of looking for conflictsbetween the actual and the required sequence at any particularpoint would itself require careful monitoring.

A difficulty in this third stage, therefore, could well relateto the general problem frontal lobe patients have in avoidingdata-driven errors, as in the capture error experiment of DellaMalva et al. (1993) or in the sentence completion errors inthe Hayling B sentence completion task (Burgess and Shallice,1996). Such problems would be exacerbated in the presenttasks in that the correct response requires the subject to setup an abstract representation of the action sequence whichmust compete for the patient’s attention with possible plaus-ible responses directly triggered by inappropriate combina-tions of cards on the table. The processes required of strategygeneration and application for a non-routine situation on theone hand and monitoring on the other, are key supervisorysubprocesses of the revised supervisory system model ofShallice and Burgess (1996). In that paper the authorsconsidered the key steps in coping with a novel situation.Strategy selection and application on the one hand, andmonitoring and checking of the resulting behaviour on theother, were two main processes for which there was evidenceof pre-frontal cortical involvement. However, assessment ofwhether impairment of this third stage or of the earlier twostages creates the sequencing difficulty will require furtherexperimentation.

The results overall show that the script sequence phen-omena described in frontal patients by Sirigu et al. (1995)are robust. However, in partial disagreement with the positionof Sirigu et al. (1998), the effects were found to generalizeacross different types of action representation. The findingsappear to be unrelated to the concept of the MKU or to thestoring of finer temporal information concerned with actions.Instead, they relate better to the general ideas of Siriguet al. (1995) and/or to a disorder of supervisory systemsubprocesses.

Acknowledgements

We would like to thank all the patients for their kindcollaboration. We are also grateful to Federica Bearzotti forhelping to collect some of the normative data and in preparingsome of the stimuli. The research was assisted by supportfrom ‘Cofinanziamento MURST’ (1998) to TS and RIR.

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Appendix 1List of 10 schema actions

Knotting a tiePreparing pastaPreparing a slice of bread with butter and jamOpening a bottle of wineWashing handsPacking a giftFilling a fountain penOpening a tin of tuna fishWashing upShaving oneself

Appendix 2List of 10 script actions

Having a meal at the restaurantGoing to the cinemaMaking a telephone call from a public telephoneGoing swimming at the swimming poolGoing to the train station to catch a trainGoing to the doctorPurchasing a dressPreparing a dinnerGoing to the market to shopGoing to fill the car with petrol

Action sequencing deficit 99

Action sequencing deficit followingfrontal lobe lesion

S. Zanini, R. I. Rumiati and T. ShalliceAbstractFrontal lobe patients carried out temporal sequencing tasks related to actionsthat differed in terms of their abstractness using both verbal and pictorialpresentations. A generalized impairment was found: neither a type of actioneffect nor a modality of item presentation effect was present. The patientsalso carried out a corresponding action production task and produced actionsquickly and without errors. The frontal lobe patients were also spared ingenerating verbal descriptions of actions: they were as accurate as normalcontrols both in terms of the details reported and in maintaining the temporalsequence. It has been argued that the difficulty in processing the temporaldimensions of actions following frontal lobe lesions is due to some form ofdisruption of the action representation. However, no action representationaldeficits were present in our frontal lobe patients. Thus, they cannot accountfor our findings. On the contrary, we suggest that the action sequencing deficitwas a consequence of the difficulties patients experienced in rejecting wrongalternatives presented by the stimulus situation.

JournalNeurocase 2002; 8: 88–99

Neurocase Reference Number:O247

Primary diagnosis of interestAction sequencing deficit

Key words: frontal lobe; sequencing; action processing

Lesion locationd Frontal lobe lesions

Lesion typeVascular, traumatic

LanguageEnglish