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Neuropsychologia 48 (2010) 1652–1663

Contents lists available at ScienceDirect

Neuropsychologia

journa l homepage: www.e lsev ier .com/ locate /neuropsychologia

onceptual proposition selection and the LIFG: Neuropsychological evidencerom a focal frontal group

ail Robinsona,∗, Tim Shalliceb,c, Marco Bozzalid,e, Lisa Cipolotti a,f

Department of Neuropsychology, National Hospital for Neurology and Neurosurgery, Queen Square, London, UKInstitute of Cognitive Neuroscience, University College, London, UKInternational School for Advanced Studies (SISSA), Trieste, ItalyWellcome Department of Imaging Neuroscience, Institute of Neurology, University College, London, UKNeuroimaging Laboratory, Santa Lucia Foundation, Rome, ItalyDepartment of Psychology, University of Palermo, Italy

r t i c l e i n f o

rticle history:eceived 18 August 2009eceived in revised form2 December 2009ccepted 5 February 2010vailable online 12 February 2010

a b s t r a c t

Much debate surrounds the role of the left inferior frontal gyrus (LIFG). Evidence from lesion and neu-roimaging studies suggests the LIFG supports a selection mechanism used in single word generation.Single case studies of dynamic aphasic patients with LIFG damage concur with this and extend the findingto selection of sentences at the conceptual preparation stage of language generation. A neuropsycholog-ical group with unselected focal frontal and non-frontal lesions is assessed on a sentence generation

eywords:erbal response selectionrefrontal cortexeuropsychology

task that varied the number of possible conceptual propositions available for selection. Frontal patientswith LIFG damage when compared to Frontal patients without LIFG damage and Posterior patients wereselectively impaired on sentence generation tests only when stimuli activated multiple conceptual propo-sitions that compete with each other for selection. We found that this selective impairment is critical forreduced speech rate, the core deficit of dynamic aphasia, and we would argue it is causative for one form

iatediple c

anguage generationynamic aphasia

of dynamic aphasia assocfor selecting among mult

The left inferior frontal gyrus (LIFG) has been implicated in lan-uage processes since the time of Broca (1861). He first claimedlink between speech output and damage to the posterior LIFG,roca’s area (Brodmann Areas [BA] 44/45). Clinical neuropsycho-

ogical studies have since suggested that LIFG damage disruptspeech production, repetition, speech fluency, reading, naming,yntactic processing, motor planning for speech, noun and verbeneration, text comprehension and propositional speech (e.g.,lexander, Benson, & Stuss, 1989; Benton, 1968; Caramazza,apitani, Rey, & Berndt, 2001; Goodglass & Kaplan, 1983; Luria,973; Milner, 1982). Thus, despite the long history of LIFG involve-ent in language processes, the precise role of the LIFG in language

eneration remains at the centre of debate.Recent lesion studies, however, suggest one role of the LIFG is

n selection for single word generation. For example, Thompson-chill et al. (1998) reported 4 patients with LIFG damage who were

Abbreviations: LIFG, left inferior frontal gyrus; LF, left frontal; RF, right frontal.∗ Corresponding author at: Department of Clinical Neuropsychology (Box 37),ational Hospital for Neurology and Neurosurgery, Queen Square, London WC1NBG, UK. Tel.: +44 207829 8793; fax: +44 2078132516.

E-mail addresses: g.robinson@ion.ucl.ac.uk, gail.robinson@uclh.nhs.ukG. Robinson).

028-3932/$ – see front matter. Crown Copyright © 2010 Published by Elsevier Ltd. All rioi:10.1016/j.neuropsychologia.2010.02.010

with LIFG lesions. These results provide evidence that the LIFG is crucialompeting conceptual propositions for language generation.

Crown Copyright © 2010 Published by Elsevier Ltd. All rights reserved.

selectively impaired in generating a single verb that had high selec-tion demands among competitors (e.g., cat—a high demand item vs.scissors—a low demand item).

In addition to single word selection, the LIFG has been impli-cated in a high-level conceptual proposition selection processnecessary for sentence generation. The assumption that a high-level selection process could be selectively impaired was based onthe investigation of two dynamic aphasic patients (ANG—Robinson,Blair, & Cipolotti, 1998; CH—Robinson, Shallice, & Cipolotti, 2005).Frontal dynamic aphasia (Luria, 1970, 1973) refers to a severeimpairment of propositional language in the context of otherwisenormal language skills (repetition, naming, comprehension, read-ing). ANG and CH both had LIFG damage. In particular there wasa striking impairment in generating sentences specifically whena stimulus activated multiple conceptual propositions that com-pete with each other for selection (e.g., sentence generation froma single common noun, table—the kitchen table, my antique table,the coffee table, the bedside table, etc.). By contrast, there was nodeficit when a stimulus that activated a dominant response (e.g.,

Proper Nouns–Ireland). The sentence (and single word) generationdeficit was accounted for by damage to the conceptual preparationstage of speech production (Levelt, 1989, 1999; Levelt, Roelofs, &Meyer, 1999), prior to lexical selection and grammatical encoding.Damage to this system was held to result in an inability to select a

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onceptual proposition from amongst competitors (for details seeobinson et al., 2005, Robinson, Shallice, & Cipolotti, 2006).

Recent work on single word selection in picture naming is some-hat related, although conceptually at a different level of the

anguage production system. Schnur, Lee, Coslett, Schwartz, andhompson-Schill (2005) and Schnur et al. (2009) conducted a grouptudy of single word selection in picture naming and identified apecific role for the LIFG. Related to these findings is the work of Jef-eries and colleagues who investigated semantic deficits in strokephasic patients using a picture naming paradigm (Jefferies, Baker,oran, & Lambon Ralph, 2007; Jefferies & Lambon Ralph, 2006;

efferies, Patterson, & Lambon Ralph, 2008). These authors arguehe semantic deficits had a refractory quality in that patients werenconsistent in the ability to ‘select and retrieve’ knowledge acrossasks, which they attributed to a failure of executive control pro-esses rather than a degradation of knowledge per se. However,hese authors report their aphasics with LIFG and temporoparietalesions were indistinguishable and “. . .both had failures of seman-ic control” (p. 656, 2008). The LIFG has also been implicated in word

eaning selection by Bedny, Hulbert, and Thompson-Schill (2007).These findings from these two types of lesion studies address-

ng selection of both conceptual propositions and lexical itemsre in keeping with neuroimaging evidence based on healthy sub-ects. The LIFG has been implicated in the selection of semanticnowledge from among competing information (Derrfuss, Brass,eumann, & Yves von Cramon, 2005; Kan & Thompson-Schill,004; Moss et al., 2005; Schnur et al., 2009; Thompson-Schill,’Esposito, Aguirre, & Farah, 1997; Thompson-Schill, D’Esposito, &an, 1999), the selection of a determiner when naming pictures

n German (Heim, Friederici, Schiller, Ruschemeyer, & Amunts,009) and selecting an appropriate meaning from multiple alter-atives in context (Bedny, McGill, & Thompson-Schill, 2008; BednyThompson-Schill, 2006; Ihara, Hayakawa, Wei, Munetsuna, &

ujimaki, 2007; Mestres-Misse, Camara, Rodriguez-Fornelis, Rotte,Munte, 2008).More critically the LIFG has been found to be involved in selec-

ion at the propositional language level (see for example Blank,cott, Murphy, Warburton, & Wise, 2002; Indefrey et al., 2001).or instance, Blank and colleagues inferred that impaired propo-itional language would arise if there was a disconnection betweenhe areas involved in a left-lateralised network (anterior left tempo-al cortex, left operculum, left superior frontal gyrus). Other typesf positions are also proposed for possible functions of the LIFG suchs top-down controlled semantic retrieval in situations where task-elevant information is not automatically made available (Badre,oldrack, Pare-Blagoev, Insler, & Wagner, 2005; Gabrieli, Poldrack,Desmond, 1998; Wagner, Pare-Blagoev, Clark, & Poldrack, 2001).Imaging studies, however, are limited. That is, a network of brain

egions sufficient to perform a selection task may become activatedut it is difficult to disentangle exactly which stage in a process nec-ssarily requires a particular brain region. By contrast, lesion dataan provide evidence for which region is necessary for a particu-ar cognitive process, and more strongly via a case series or grouptudy.

To the best of our knowledge there has been no group studyddressing the specific role of the LIFG in the selection of concep-ual propositions for sentence generation. This was investigatedn a sample of 47 patients with unselected focal frontal lesionsnd 20 patients with posterior lesions. Based on the performancef dynamic aphasic patients on sentence generation tests, it isredicted that the number of competing propositions will affect

erformance for patients with lesions to the LIFG in the followingay:

. Counter-intuitively, for patients with LIFG damage, sentencegeneration will be impaired for high frequency words. This is

gia 48 (2010) 1652–1663 1653

because high frequency words have multiple referents that acti-vate many conceptual propositions that compete with eachother for selection.

2. By contrast, for patients with LIFG damage, sentence generationwill be relatively unimpaired for low frequency words. Low fre-quency words have fewer referents than high frequency wordsand hence activate few or a dominant conceptual proposition(s).Of note, this is the first time low frequency words have been usedin sentence generation tests.

3. Further, for patients with LIFG damage, sentence generation willbe unimpaired for Proper Nouns. Proper Nouns have a singularor few referents and should strongly activate a single prepotentconceptual proposition.

4. The stimulus feature of competition between multiple concep-tual propositions, as activated by high frequency words, will notaffect the sentence generation performance of frontal patientswithout LIFG damage or posterior patients, including left tem-poral patients.

1. Materials and methods

1.1. Subjects

Seventy-two patients with focal lesions were recruited from the National Hos-pital for Neurology and Neurosurgery. Patients met the following inclusion criteria:(1) Presence of a focal frontal or non-frontal lesion (see below for details) due to dif-ferent possible aetiologies including; brain tumour, stroke, haemorrhage, subduralhaematoma and one traumatic brain injury patient; (2) Availability of a MRI or CTscan; (3) No prior neurological or psychiatric history; (4) English as the primary lan-guage; (5) No history of learning disability. Patients were excluded if: (1) Significantcognitive impairments (receptive aphasia, alexia, neglect) or behavioural problemsconfounded the ability to participate in testing; (2) MRI scans showed concomi-tant widespread pathology (e.g., diffuse cerebral vascular disease) or more than twohyperintense areas with a diameter ≥ 10 mm or more than eight hyperintense areaswith a diameter between 5 and 9 mm on dual-echo images (in addition to the singlefocal lesion). Reviewing CT scans that are less sensitive to widespread pathology,all subjects showing any additional abnormality were excluded. Of the seventy-twopatients, five were excluded due to their concomitant frontal and posterior involve-ment. This left forty-seven patients with focal frontal lesions and twenty patientswith posterior lesions. A description of patients’ lesion location, aetiology, lesionextent and chronicity is available in Appendix A. The patients were compared tothirty-five healthy adult controls with no neurological or psychiatric history. Con-trols were recruited to match the patient group as closely as possible for age, genderand education.

Patients were tested either at hospital whilst an inpatient or outpatient, orin their home. Approval for the study was granted by the National Hospital forNeurology and Neurosurgery and the Institute of Neurology Joint Research EthicsCommittee and the University College London Hospitals NHS Trust Research andDevelopment Directorate. All subjects gave informed written consent to take partin the study, and were allowed to withdraw at any time.

1.2. Lesion analyses

The lesion localisation method included the standard anatomical classificationand an adapted version of the lesion localisation and statistical procedures outlinedby Turner, Cipolotti, Yousry, and Shallice (2007) that was based on an approachdeveloped by Stuss et al. (2002). A Neurologist (MB) who was blind to the neurolog-ical history of each patient, and unaware which scan belonged to whom, reviewedthe hard copies of the MRI scans for each patient (or CT where MRI was unavailable,n = 14). Brain MRI was obtained on systems operated at 1.5 T, and included the acqui-sition of an axial dual-echo, and an axial and coronal T1-weighted scan. Both MRIand CT data were used as our goal for lesion assessment was to enable the recruit-ment of a large number of patients. Thus neuroimaging data collected for clinicalpurposes in different centres was used. Nevertheless, the guidelines used for exclu-sion criteria and lesion assessment were rigorous, and based on a relatively detailedanatomical localisation. The position of every lesion was labelled using standardatlases (Duvernoy, 1991). Frontal patients were identified as those with a lesionin any part of the brain anterior to the central sulcus and superior to the lateralfissure, including cases with dorsal striatum lesions. Posterior lesions were codedas broadly falling within the temporal, parietal and/or occipital lobes. Each frontal

patient was coded for the presence of lesion and oedema in each hemisphere in 9frontal regions (18 areas in total): inferior frontal gyrus (anterior/posterior); middlefrontal gyrus (anterior/posterior); and superior frontal gyrus (anterior/posterior);cingulate cortex (anterior/posterior); and orbital cortex. On the lateral surface theanterior/posterior border was taken as the point midway between the frontal poleand the central sulcus. On the medial surface the anterior/posterior border was

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taken as the point midway between the frontal pole and the ramus marginalis. Lesionextent was calculated for each frontal patient based on the number of frontal regionsinvolved. For a subset of frontal patients for whom electronic imaging was available(n = 14), lesion volume was calculated. For each subject, lesion size was measuredon T2-w scans using a semi-automated local thresholding contouring software (Jim4.0, Xinapse System, Leicester, UK. http://www.xinapse.com/).

1.3. Behavioural analyses

The 18 frontal regions were collapsed into groups in three different ways forgroup comparisons. In the 1st Analysis (Frontal vs. Posterior vs. Controls), all 18 regionswere collapsed together to establish a general frontal effect (Frontal: n = 47; Poste-rior: n = 20, 12 Left 8 Right; Controls: n = 35). In the 2nd Analysis (Left Frontal vs.Right Frontal vs. Controls), the 9 regions within each hemisphere were collapsedto establish a lateralisation effect (Left Frontal (LF): n = 18, Right Frontal (RF): n = 22,Controls: n = 35; NB: 7 Frontal patients were excluded as their lesions included areasfrom both the Left and Right Frontal region). The 2nd analysis enables our findingsto be compared with studies using the common left and right anterior frontal classi-fication. The 3rd Analysis (Left Inferior Frontal Gyrus vs. Non-Left Inferior Frontal Gyrusvs. Controls) was specifically designed to investigate the hypothesis that the LIFGunderpins the ability to select between multiple competing conceptual proposi-tions. Thus, Frontal patients with any part of their lesion in the anterior or posteriorsection of the left inferior frontal gyrus (n = 12) were compared to patients withlesions in the remaining 16 frontal regions, that is patients without LIFG lesions(Non-LIFG: n = 35) and Controls (n = 35).

1.4. Behavioural measures

1.4.1. Cognitive testsAll subjects were assessed on baseline cognitive and language tests. This

included measures of pre-morbid level of intelligence (National Adult ReadingTest—Nelson & Willison, 1991), current intellectual ability (Advanced ProgressiveMatrices, APM—Raven, 1976), verbal and visual memory (Recognition MemoryTest, RMT—Warrington, 1984), executive functioning (phonemic word fluency;Hayling Sentence Completion Test—Burgess & Shallice, 1997), spontaneous speech(complex scene description), repetition (3–6 word sentences,/10), naming (GradedNaming Test—McKenna & Warrington, 1980) and word comprehension (SynonymTest—Warrington, McKenna, & Orpwood, 1998). For the complex scene (BeachScene), subjects were asked to describe the contents (maximum time = 1 minute).Each speech sample was recorded and clinically characterised as normal/abnormalalong three dimensions: syntax (structure and grammar within a sentence); fluency(number of connected sentences); and dysphasic errors (semantic, phonological).

1.5. Experimental sentence generation tests

The experimental sentence generation tests consisted of the following stimuli:(i) 15 high frequency words [HFW] (e.g., water; M = 425, Kucera & Francis, 1982);(ii) 15 low frequency words [LFW] (e.g., kite; M ≤ 1, Kucera et al., 1982); and (iii)15 proper nouns [PN] (e.g., Hitler) (stimuli in Appendix B). The number of repeatedand other conceptual propositions activated by each stimuli type was investigatedin healthy controls (n = 15). Each stimulus was randomly presented to controls whowere asked to generate a meaningful sentence that incorporated the target word.The main idea of each sentence was classified by two research assistants (blind to thepurpose of the study). If more than one control generated a sentence with the samereferent it was classified as a specific repeated conceptual proposition. If only onecontrol referred to a topic in a sentence it was classified as other. The mean numberof repeated and other conceptual propositions activated by each word stimuli typediffered significantly (HFW: repeated M = 4.3, S.D. = 1.0, other M = 6.1, S.D. = 1.6; LFW:repeated M = 9.2, S.D. = 1.9, other M = 2.2, S.D. = 0.8; PN: repeated M = 8.0, S.D. = 1.7,other M = 2.3, S.D. = 1.4; repeated and other both P < 0.001: pairwise comparisons forrepeated HFW < LFW and PN, both P < 0.001, LFW > PN, P = 0.037, n.s. after Bonfer-onni correction for multiple comparisons; other HFW > LFW and PN, both P < 0.001,LFW = PN, P = 0.735). With regard to other linguistic variables, high and low fre-quency words were equivalent along the dimensions of imageability (HFW: M = 536,S.D. = 96; LFW: M = 588, S.D. = 31; P = 0.301) and syllable length although both wereshorter when compared to Proper Nouns (HFW: M = 1.7, S.D. = 0.7; LFW M = 2.1,S.D. = 0.7; PN: M = 3.1, S.D. = 1.0; P < 0.001; pairwise comparisons PN > HFW, P < 0.001;PN > LFW, P = 0.002; HFW = LFW, P = 0.13).

As with the control study, subjects were randomly presented with each stimulusand asked to produce a meaningful sentence that incorporated the target word. Theability to generate a sentence, regardless of grammatical correctness, was scoredas correct. Number correct and mean response time (RT) were recorded. RT wasdefined as the time from the end of stimulus presentation to the start of responsegeneration. Mean RT was calculated for correct responses only.

1.6. Statistical analyses

Analysis of variance (ANOVA) was used for the 1st Analysis comparing patientgroups to Controls, with Posterior patients included as a whole group. Where signif-icant differences emerged, additional analyses were conducted to investigate Left

G. Robinson et al. / Neuropsychologia 48 (2010) 1652–1663 1655

Table 2aBaseline Cognitive Tests: Mean Scores (S.D.) for Healthy Controls, Posterior Patients (Left and Right) and Frontal Patients (1st Analysis), with statistics shown.

1st Analysis

Healthy Controls Posterior Patients Frontal Patients

N = 35 All Left Right N = 47N = 20 N = 12 N = 8

Advanced Progressive Matrices(/12)

7.56 (3.0) 7.32 (2.4) 6.58 (2.9) 7.88 (2.4) 6.58 (2.9)

F(2,88) = 1.14, P > 0.05

Recognition Memory Test Words(/50)

45a 44.7 (4.7) 42.9 (4.5) 48.8 (1.9) 44.7 (5.0)

t(52) = −0.02, P > 0.05

Faces (/50) 44a 41.1 (6.0) 41.7 (6.3) 39.8 (6.2) 40.1 (6.0)t(52) = −0.53, P > 0.05

Hayling Overall Scoreb 6.19 (1.1) 5.47 (1.4) 5.90 (0.7) 4.86 (2.0) 3.98*** ,c (2.1)�2

(2)= 23.72, P < 0.001

Phonemic Word fluency 26.1 (7.7) 21.3 (8.2) 20.8 (7.9) 22.0 (9.2) 14.3*** ,b (8.8)F(2,99) = 20.45, P < 0.001

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*** P < 0.001, compared to Healthy Controls and All Posterior Patients.

nd Right Posterior differences. In the 2nd Analysis comparing LF and RF patientso Controls, univariate analysis of covariance (ANCOVA) was used with Age entereds a covariate. In the 3rd Analysis comparing LIFG and Non-LIFG frontal patients toontrols, an ANCOVA was used with Lesion Extent entered as a covariate. Signifi-ant results were followed by pairwise comparisons using Bonferroni’s correctiono adjust for multiple comparisons (e.g., P ≤ 0.017). In those cases where Leveneests showed error variances between groups differed significantly, data were trans-ormed using the logarithm. If error variances remained unequal non-parametrictatistics were applied (Kruskal-Wallis Test �2). Significant Kruskal-Wallis Testsere followed by pairwise Mann–Whitney U Tests. The Chi-square test of inde-endence was used for categorical data (e.g., sex and spontaneous speech).

. Results

.1. Descriptive characteristics summary

Control and patient groups did not differ significantly in termsf sex or pre-morbid intelligence for any level of analyses (i.e., 1stnalysis: Frontal vs. Posterior vs. Controls; 2nd Analysis: LF vs.F vs. Controls; 3rd Analysis: LIFG vs. Non-LIFG vs. Controls; all> 0.05; see Table 1). There was also no difference in Age betweenroups in the 1st and 3rd Analyses, although in the 2nd Analysishe RF group was significantly older than the LF group (U = 91.000,= 0.004). Thus, age was entered as a covariate for the 2nd Analy-es. The time since the lesion occurred was equivalent in all frontalub-groups (i.e., 2nd and 3rd Analyses); however, Posterior patientsere more acute than Frontal patients (1st Analysis; U = 169.000,= 0.006). Lesion Extent for the LIFG group was larger than theon-LIFG Group (t(45) = 2.361, P = 0.023), thus, it was entered ascovariate in the 3rd Analyses. For the sub-set of patients forhom electronic imaging was available (n = 14), lesion volumeas equivalent across the critical frontal sub-groups (LIFG [n = 4]= 5330.9 mm2, S.D. = 3697.8; Non-LIFG [n = 10] M = 5076.8 mm2,

.D. = 6142.9; t(12) = 0.076, P = 0.940).

.2. Cognitive and language baseline summary

The mean scores with standard deviations and statistics for allognitive baseline tests are contained in Tables 2a and 2b. The

rontal group (and all frontal sub-groups) performed normally onntellectual and verbal memory tests. The Frontal and Posterioratients performed in the lower normal range on the facial mem-ry test. Notably, there was no difference between frontal patientsith and without LIFG damage and, in general, the frontal patients

stical Analysis.

ts for the Hayling).

present with relatively mild global deficits. As expected, a Frontaldeficit was documented on executive tests. More specifically, on theHayling the performance of all frontal sub-groups was impaired. Asevere Frontal deficit was found for Phonemic Word Fluency, con-firming the sensitivity of the generative aspect of word fluency teststo frontal lesions.

The mean scores with standard deviations and statistics for alllanguage baseline tests are contained in Tables 3a and 3b. Overall,apart from spontaneous speech, Frontal patients performed wellon baseline language tests. A significant number of Frontal patientspresented with agrammatic and non-fluent speech containing dys-phasic errors. In addition mild nominal and comprehension deficitswere present and, as expected, Left Posterior patients showeda mild nominal deficit. Although the LF patients were generallypoorer than RF patients, it was important there was no differencebetween the critical LIFG and Non-LIFG frontal sub-groups. Readingskills were normal. The absence of significant nominal, comprehen-sion and reading deficits in Frontal patients concurs with previouslesion studies of language, including dynamic aphasia.

2.3. Experimental Tests: Sentence Generation from a Single Word

2.3.1. 1st Analysis: frontal vs. posterior vs. controlsThe number of sentences generated from a single word dif-

fered significantly between the Frontal, Posterior and Controlgroups. This difference was evident for each stimuli type includ-ing High Frequency words [HFW] (�2

(2) = 10.657, P = 0.004), Low

Frequency words [LFW] (�2(2) = 7.006, P = 0.026) and Proper Nouns

[PN] (�2(2) = 7.297, P = 0.024) (see Table 4). Frontals generated

fewer sentences when presented with HFW than both Controls(P = 0.015) and Posteriors (P = 0.014). In addition, Frontals gener-ated fewer sentences to LFW than Posteriors (P = 0.007) but notControls (P = 0.438). By contrast, as expected, there were no spe-cific group effects for PN stimuli. There were no group differencesfor the time taken (RT) to generate sentences for any word type(HFW: F(2,98) = 1.640, P = 0.256; LFW: F(2,98) = 1.537, P = 0.216; PN:

F(2,98) = 1.616, P = 0.256).

2.3.1.1. Sentence generation tests and executive function measures.The sentence generation tests and executive function measures(Phonemic fluency, Hayling) require a generation component, and

1656 G. Robinson et al. / Neuropsychologia 48 (2010) 1652–1663

Table 2bBaseline Cognitive Tests: Mean Scores (S.D.) for Healthy Controls and Frontal Sub-Groups for 2nd Analysis (Left, Right) and 3rd Analysis (LIFG, Non-LIFG), with statisticsshown for each Analysis.

2nd Analysis 3rd Analysis

Healthy Controls Frontal Sub-Groups Frontal Sub-Groups

N = 35 LF RF LIFG Non-LIFGN = 18 N = 22 N = 12 N = 35

Advanced Progressive Matrices(/12)

7.56 (3.0) 8.24 (2.3) 6.14 (2.8) 7.55 (2.7) 6.26 (2.9)

F(2,61) = 0.89, P > 0.05 F(2,68) = 1.31, P > 0.05Age F(1,61) = 12.9, P < 0.01

Recognition Memory TestWords (/50)

45a 46.4 (3.3) 44.2 (5.7) 44.8 (3.5) 44.6 (5.4)

F(1,32) = 0.52, P > 0.05 t(39) = 0.10, P > 0.05

Faces (/50) 44# 43.1 (3.5) 37.7*,a (6.8) 41.7 (3.7) 39.6 (6.5)U = 72.50, P < 0.05 t(39) = 0.99, P > 0.05

Hayling Overall Scoreb 6.19 (1.1) 4.29** (2.1) 3.62*** (2.0) 4.40* (2.2) 3.85*** (2.0)�2

(2)= 22.94, P < 0.001 �2

(2)= 22.76, P < 0.001

Phonemic Word fluency 26.1 (7.7) 9.7*** ,a (8.0) 18.4** (6.2) 7.8*** ,a (7.9) 16.6*** (8.0)F(2,71) = 29.96, P < 0.001 F(2,78) = 8.71, P < 0.001

LF = Left Frontal; RF = Right Frontal; LIFG = Left Inferior Frontal Gyrus. Covariates are Age in 2nd Analysis and Lesion Extent in 3rd Analysis.a Compared to both Healthy Controls and the patient group in the analysis.

tsfotPreplno

TBw

b Scaled Score is 1–10, 6 is average.* P < 0.05, compared to Healthy Controls.

** P < 0.01, compared to Healthy Controls.*** P < 0.001, compared to Healthy Controls.

herefore these tasks were hypothesised to tap, at least in part,imilar processes. We investigated the relationship between per-ormance on sentence generation for each stimulus type and thatf phonemic fluency and the Hayling. As expected, significant posi-ive correlations were found (HFW—Phonemic Fluency, r = 0.415,< 0.001, Hayling, r = 0.365, P < 0.001; LFW—Phonemic Fluency,= 0.341, P < 0.001, Hayling, r = 0.274, P = 0.008; PN—Phonemic Flu-

ncy, r = 0.334, P = 0.001, Hayling, r = 0.326, P = 0.002). Thus, aatient who performs well on the sentence generation test is also

ikely to perform well on phonemic fluency and the Hayling. Ofote, correlations did not reach significance between performancen sentence generation tests and other cognitive baseline measures

able 3aaseline language tests: number of patients with abnormal spontaneous speech and meanith statistics shown.

1st Analys

Healthy Controls Posterior P

N = 35 AllN = 20

Spontaneous Speecha

Agrammatical Speech 0 0�2

(3)= 10.1

Non-fluent Speech 0 0�2

(3)= 18.9

Errors Semantic: Phonological 0:0 4:0**

�2(6)

= 18.1

Sentence Repetition (/10) 10 (0) 10 (0)�2

(3)= 10.0

Graded Naming Test (/30) 22.3 (4.9) 17.8* (7.4)F(2,97) = 4.8

Synonyms Test (/50) 43.1 (6.8) 43.4 (5.2)F(2,92) = 3.1

a No. of patients with abnormal spontaneous speech.b Compared to both Healthy Controls and the patient group in the analysis (Left Poster* P < 0.05, compared to Healthy Controls.

** P < 0.01, compared to Healthy Controls.*** P < 0.001, compared to Healthy Controls.

that were not predicted to be related (e.g., HFW and verbal andvisual recognition memory, P > 0.05).

2.3.2. 2nd Analysis: left frontal vs. right frontal vs. controlsThe LF and RF patients and Controls performed equivalently on

experimental tasks apart from the LF patients’ poorer performance

than Controls, but not RF patients, in the number of sentencesgenerated for HFW (�2

(2) = 7.642, P = 0.022; Pairwise comparisons:LF < Controls, P = 0.007; LF = RF, P = 0.131; see Table 4). Thus, therewas no difference in the number of sentences generated for LFW(F(2,71) = 0.099, P = 0.906) or PN (�2

(2) = 3.810, P = 0.149) or in RTs

scores (S.D.) for Healthy Controls, Posterior Patients, Frontal Patients (1st Analysis),

is

atients Frontal Patients

Left Right N = 47N = 12 N = 8

0 0 8*

6, P < 0.05

0 0 14*** ,b

9, P < 0.001

4:0** 0:0 4:38, P < 0.01

10 (0) 10 (0) 9.57* (1.3)4, P < 0.05

15.0*** (8.1) 22.0 (3.3) 18.8**,b (5.6)7, P < 0.05

42.2 (6.0) 45.0 93.5) 39.7* (7.2)8, P < 0.05

ior for the Graded Naming Test).

G. Robinson et al. / Neuropsychologia 48 (2010) 1652–1663 1657

Table 3bBaseline language tests: number of patients with abnormal spontaneous speech and mean scores (S.D.) for Healthy Controls and Frontal Sub-Groups for 2nd Analysis (Left,Right) and 3rd Analysis (LIFG, Non-LIFG), with statistics shown for each Analysis.

2nd Analysis 3rd Analysis

Healthy Controls Frontal Sub-Groups Frontal Sub-Groups

N = 35 LF RF LIFG Non-LIFGN = 18 N = 22 N = 12 N = 35

Spontaneous Speecha

Agrammatical Speech 0 5**,b 1 2* 6*

�2(2)

= 12.97, P < 0.01 �2(2)

= 6.60, P < 0.05

Non-fluent Speech 0 5** 5** 5*** 9**

�2(2)

= 10.32, P < 0.01 �2(2)

= 14.18, P < 0.01

Errors Semantic: Phonological 0:0 4:2**,b 0:0 4:1*** 0:2�2

(2)= 20.65, P < 0.001 �2

(4)= 27.48, P < 0.001

Sentence Repetition (/10) 10 (0) 9.28*** ,b (1.5) 9.95 (0.2) 9.17*** (1.8) 9.17* (1.1)�2

(2)= 16.46, P < 0.001 �2

(2)= 11.30, P < 0.01

Graded Naming Test (/30) 22.3 (4.9) 17.9* (4.8) 19.7 (5.9) 16.8 (5.3) 19.5 (5.7)F(2,69) = 4.14, P < 0.05 F(2,76) = 0.54, P > 0.05

Synonyms Test (/50) 43.1 (6.8) 36.9** (7.6) 41.5 (6.8) 37.3 (8.8) 40.6 (6.4)F(2,66) = 3.94, P < 0.05; Age F(1,66) = 9.67, P < 0.01 F(2,72) = 1.10, P > 0.05

LF = Left Frontal; RF = Right Frontal; LIFG = Left Inferior Frontal Gyrus. Covariates are Age in 2nd Analysis and Lesion Extent in 3rd Analysis.a No. of patients with abnormal spontaneous speech.

(F

2f

trptpcaP

TEF

L

b Compared to both Healthy Controls and the patient group in the analysis.* P < 0.05, compared to Healthy Controls.

** P < 0.01, compared to Healthy Controls.*** P < 0.001, compared to Healthy Controls.

HFW: F(2,71) = 1.245, P = 0.294; LFW: F(2,71) = 1.476, P = 0.236; PN:(2,71) = 1.389, P = 0.256).

.3.3. 3rd Analysis: left inferior frontal gyrus vs. non-left inferiorrontal gyrus vs. controls

For this level of analysis, it was a specific theoretical predictionhat only patients with a lesion involving the left inferior frontalegion would be affected by the number of activated conceptualropositions. Thus, when a stimulus activates multiple concep-

ual propositions such as for high frequency words [HFW], LIFGatients should perform worse as they are unable to select betweenompeting conceptual propositions. By contrast, when a stimulusctivates few (i.e., low frequency words [LFW]) or a dominant (i.e.,roper noun [PN]) conceptual proposition(s), LIFG patients should

able 4xperimental Sentence Generation Tests: Mean Score (Max = 15), Response Time and Starontal Sub-Groups for 2nd Analysis (Left, Right) and 3rd Analysis (LIFG, Non-LIFG).

Word type Healthy Controls 1st Analysis

N = 35 Posterior Patients Frontal Patient

N = 20 N = 47

High FrequencyScore 14.9 (0.2) 15.0 (0.0) 13.8*,b (3.2)RT 2.6 (1.6) 2.6 (1.5) 4.5 (7.5)

Low FrequencyScore 14.5 (1.1) 15.0 (0.0) 14.0**,c (2.5)RT 2.3 (1.5) 2.0 (0.9) 4.0 (7.4)

Proper NounsScore 15.0 (0.2) 15.0 (0.0) 14.5 (1.6)RT 2.4 (1.7) 1.9 (0.7) 3.5 (5.0)

F = Left Frontal; RF = Right Frontal; LIFG = Left Inferior Frontal Gyrus; RT = Response Timea Posterior Patients are not divided into Left and Right Posterior groups as all patients pb Compared to both Healthy Controls and the patient group in the analysis (1st—Posterc Compared to Posterior patients only.* P < 0.05.

** P < 0.01.*** P < 0.001.

be unimpaired as there is no competition or need for a selectionmechanism in order to generate a sentence.

As predicted, there was a significant difference in the numberof sentences generated between the LIFG, Non-LIFG and Controlgroups only when presented with HFW (�2

(2) = 17.557, P < 0.001;see Table 4 and Fig. 1). Pairwise comparisons showed that, com-pared to Controls, only the LIFG group generated fewer sentenceswhen presented with HFW (P < 0.001). Importantly, the LIFG groupalso generated significantly fewer sentences than the Non-LIFG

frontal group (P < 0.005). By contrast, no difference was revealedbetween groups when presented with stimuli that activate fewor a dominant conceptual proposition; that is, for both LFW(F(2,78) = 1.037, P = 0.359) and PN (�2

(2) = 4.199, P = 0.122), althoughlesion extent was a significant covariate for LFW (P < 0.006). There

ndard Deviations (S.D.): Healthy Controls, Posterior Patientsa, Frontal Patients and

2nd Analysis 3rd Analysis

s Frontal Sub-Groups Frontal Sub-Groups

LF RF LIFG Non-LIFGN = 18 N = 22 N = 12 N = 35

13.9** (2.7) 14.7 (0.9) 13.0*** ,b (3.2) 14.1 (3.2)3.3 (3.0) 3.7 (2.6) 3.6 (3.5) 4.8 (8.4)

14.3 (1.4) 14.5 (0.9) 13.8 (1.7) 14.0 (2.8)3.5 (5.2) 2.5 (1.1) 4.1 (6.4) 4.0 (7.9)

14.8 (0.5) 14.8 (0.5) 14.8 (0.6) 14.4 (1.8)3.4 (4.9) 2.5 (1.3) 4.0 (5.9) 3.3 (4.8)

.erformed equivalently on each test.ior; 3rd—Non-LIFG).

1658 G. Robinson et al. / Neuropsychol

Fig. 1. Generation of a Sentence from a Word: Mean Number Correct (Max = 15) foreach Word Type (High Frequency words, Low Frequency words, Proper Nouns) forFLfa

wfFlPt

2tmrieihoiHptFtn1

2ioe(PNpisswlc

rontal patients with and without Left Inferior Frontal Gyrus damage (LIFG and Non-IFG) and Healthy Controls. The LIFG patients mean number of sentences generatedor high frequency words was significantly lower than both the Non-LIFG patientsnd Controls (denoted by *).

ere no group differences in the time taken to generate sentencesor any type of word stimuli (HFW: F(2,78) = 1.736, P = 0.0183; LFW:(2,78) = 1.044, P = 0.357; PN: F(2,78) = 0.721, P = 0.489), althoughesion extent was significant for RT for each stimuli (F(1,78) = 9.101,= 0.003, F(1,78) = 8.470, P = 0.005, F(1,78) = 7.110, P = 0.009, respec-

ively).

.3.3.1. Error analysis. The 12 LIFG patients produced 39 errors inotal (Errors by stimuli type: HFW = 22; LFW = 13; and PN = 4). The

ajority of errors were omissions (i.e., No Response or ‘I Don’t know’esponses; 61.5%; e.g., no response given for ‘water’). More specif-cally, for each word type omission errors comprised 68% of HFWrrors, 54% of LFW errors and 50% of PN errors. Production of anncomplete sentence was the next most common error (e.g., Theelmet was. . .. for ‘helmet’; 20.5%) and specifically comprised 18%f HFW errors, 15% of LFW errors and 50% of PN errors. The remain-ng errors were a 1-word response rather than a sentence for twoFW stimuli (e.g., me for ‘man’ and Teresa for ‘mother’; 5%) and oneatient produced a phonological (and perseverative) response forhe HFW stimuli ‘face’ (e.g., Forty, face, forty . . . um I don’t know).inally, four LFW errors consisted of patients not understanding thearget word meaning presumably as the low frequency item wasot within their vocabulary (for ‘leotard’ ‘pagoda’ ‘tutu’ ‘thimble’;0% of total errors and 31% of LFW errors).

.3.3.2. Lesion size. As lesion extent was a significant covariaten each parametric analysis we will specifically address whetherbtained effects could be due to lesion extent for the analyses whererror variances were unequal, requiring non-parametric statisticsi.e., Kruskal Wallis �2 Test for high frequency word scores androper Noun scores). As there was no group difference for Properouns the main question is whether the significantly impairederformance of the LIFG Frontals for high frequency words, the crit-

cal condition, was due to lesion extent rather than a failure of a

election mechanism when there is competition. The LIFG Frontalub-group was divided into 2 groups by lesion extent. LIFG patientsith >5 frontal areas damaged were classified as having ‘Large’

esions (n = 6). LIFG patients with ≤5 frontal areas damaged werelassified as having ‘Small’ lesions (n = 6). First, the ‘Small’ lesion

ogia 48 (2010) 1652–1663

group had a lower mean high frequency word score (M = 12.17,S.D. = 4.26) than the Non-LIFG Group (M = 14.1, S.D. = 3.2). Thus, LIFGpatients with small lesions performed more poorly than Non-LIFGpatients. Moreover, the mean high frequency word score of the‘Small’ lesion LIFG group was lower than the ‘Large’ lesion group(M = 13.83, S.D. = 1.60). Thus, LIFG patients with larger lesions per-formed better on the critical test. The mean scores of LIFG patientswith large and small lesions was identical for low frequency words(M = 13.83) and almost the same for Proper Nouns (Large: M = 14.67;Small: M = 14.83). The high frequency effects obtained cannot plau-sibly be attributed to lesion size. This conclusion of the specificityof the high frequency effects is strongly supported by the equiva-lent mean lesion volume of the sub-set of frontal patients for whomelectronic data was available (n = 14; see above in the descriptivecharacteristics summary).

2.3.3.3. Sentence generation and left inferior frontal and temporallesions. Given that both the LIFG and left temporal cortex are impli-cated in language production processes (e.g., Maess, Friederici,Damian, Meyer, & Levelt, 2002) and lesions to both these areashave been argued to result in executive control process deficits(e.g., Jefferies et al., 2008), additional analyses were conductedthat directly compared these two patient groups. Of note, eachLeft Temporal patient (n = 6) performed this task flawlessly foreach stimuli type (HFW, LFW and PN all M = 15.0, S.D. = 0). Asvariances were unequal, non-parametric Mann–Whitney U com-parisons were used with no significant group difference in thenumber of sentences generated for LFW (U = 21.000, P = 0.075) orPN (U = 30.000, P = 0.303). By contrast, LIFG patients generatedfewer sentences for HFW than Left Temporal patients (U = 15.000,P = 0.025). There were no significant group differences in RTs forany stimuli type (HFW: t(16) = 1.125, P = 0.277; LFW: t(16) = 0.938,P = 0.362; PN: t(16) = 1.024, P = 0.321).

2.3.3.4. Sentence generation and dynamic aphasia. The core deficitof dynamic aphasia is severely reduced spontaneous speech.We have previously described two subtypes of dynamic apha-sia (Robinson et al., 1998, 2005, 2006). The less documented 2ndsubtype of dynamic aphasia is reported in patients with bilateralfrontal and subcortical damage and may involve additional non-verbal generation deficits. Word and sentence level generationtests are typically performed well but discourse level genera-tion tests are failed (e.g., Robinson et al., 2006). The 1st subtypeof dynamic aphasia is documented in patients with LIFG lesionsand is characterised by an impairment on sentence (and singleword) generation tests when a stimulus activates many compet-ing conceptual propositions, such as for high frequency words(Robinson et al., 1998, 2005). Therefore, we hypothesised that forpatients with LIFG lesions performance on the sentence genera-tion tests would be related to the spontaneous speech measure forthe condition critical for selection between competing conceptualpropositions (i.e., HFW). Thus, for the LIFG patients two measureswere calculated from the Number of Correct responses on sentencegeneration tests: (1) HFW score–LFW score; and (2) HFW score–PNscore. These two measures that contrast performance on high fre-quency words with that of the other two theoretically non-criticalconditions were correlated with spontaneous speech rate (wordsper minute) using a non-parametric correlation (Spearman’s rho).Strikingly the results confirm that the two sentence generation con-trast measures were significantly positively correlated with speechrate (see Table 5). That is, the more reduced the speech rate the

poorer the ability to generate a sentence from a HFW when con-trasted either with LFW or PN. The correlations were repeatedexcluding the 2 LIFG patients who were rated as having agrammaticspontaneous speech. Remarkably, the correlations remained signif-icant suggesting that this deficit in an inability to select between

G. Robinson et al. / Neuropsychologia 48 (2010) 1652–1663 1659

Table 5Correlation of sentence generation contrast measures and speech rate for LIFG patients (total group, N = 12, and with agrammatic patients excluded, N = 10).

Sentence generation contrast measures (difference score for number correct) Speech rate of LIFG patients

Whole group (N = 12) Excluding agrammatic patients (N = 10)

High Frequency–Low Frequency Score r = 0.636 r = 0.874P = 0.026 P = 0.001

High Frequency–Proper Nouns Score r = 0.758 r = 0.820

r

cs

3

nsigtswrcufoaoTgttsc

fgtastoGiBa2shtemLoghtttea

= Spearman’s rho non-parametric correlation.

ompeting conceptual propositions when generating a sentence,uch as for HFW, is in addition to any grammatical impairment.

. Discussion

This study investigated the role of the LIFG in one mecha-ism involved in propositional language generation; namely, theelection of conceptual propositions for sentence generation. Thiss the first investigation of conceptual proposition selection in aroup of patients with unselected focal frontal lesions. A selec-ive LIFG deficit was found for sentence generation only whentimuli activated multiple conceptual propositions that competeith each other for selection (high frequency words). This was

egardless of whether sentences were grammatically correct. Byontrast, no deficit was observed for the LIFG patients from stim-li that activated few or a dominant conceptual proposition (lowrequency words, Proper Nouns). Moreover, frontal patients with-ut LIFG damage and Posterior patients, including left temporalnd parietal patients, were unimpaired regardless of the numberf possible conceptual propositions (i.e., many, few or a dominant).hus, the LIFG was crucial in conceptual propositional languageeneration when selection was required. Interestingly, this sen-ence generation impairment for high frequency words was showno relate to reduced speech rate, the hallmark of dynamic apha-ia. The present findings suggest that lesions involving the LIFG areritically involved in the causation of dynamic aphasia.

Can our findings be accounted for by alternative explanationsor the function of the LIFG? First, it is unlikely that other lan-uage deficits underpin the LIFG patients’ performance given thathe baseline language assessment demonstrated good (or equiv-lent) naming and comprehension skills in the critical frontalub-groups. With regard to the complex process of on-line sen-ence construction, the LIFG has been implicated in the productionf syntactically complex sentences (see for review Caplan, 2006;rodzinsky, 2000). For instance, studies relating syntactic process-

ng to the LIFG include ones of verb production in patients withroca’s aphasia (e.g., Hillis, Tuffiasch, & Caramazza, 2002), of verbrgument structure in sentence production (e.g., Lee & Thompson,004; Shapiro, Gordon, Hack, & Killackey, 2002) and of agrammaticpeech. Thus, a recent study of a stroke patient with temporaryypoperfusion of Broca’s region provides specific evidence thathe LIFG is critical for production of grammatical sentences (Davist al., 2008). However, any impairment of this process should beanifest in the syntax measure. Interestingly the majority of our

IFG patients did not present with agrammatic speech. Moreoverur most critical measure with respect to propositional languageeneration when selection is required is sentence generation fromigh frequency words. The two measures that specifically contrast

he LIFG patients’ ability on this critical measure with the otherwo conditions correlate significantly with speech rate, a reduc-ion being the hallmark of dynamic aphasia. Strikingly, the sameffects occur when the two agrammatic patients with LIFG lesionsre removed. We have previously argued that in dynamic aphasia

P = 0.004 P = 0.004

the impaired selection process for the generation of new conceptsoccurs at Levelt’s conceptual preparation stage, prior to the stageat which propositions are specified in syntactic and lexical formto subsequently be realised as overt speech (Robinson et al., 2005;Warren, Warren, Fox, & Warrington, 2003).

With regard to an executive impairment explanation, both theLIFG and Non-LIFG patients were equally impaired on certainexecutive measures (e.g., Hayling). Thus, although generation (orinitiation) deficits are well documented in the context of frontallobe damage (Milner, 1982), this explanation cannot account for theselectivity of the sentence generation deficit specifically in the LIFGgroup. Finally, can our findings be attributed to reduced activationlevels rather than a failure in a selection mechanism? If this werethe case, it is not clear what prediction should be made; perhapsthe opposite pattern would occur. That is, when many options areavailable (i.e., for high frequency words) there would be a higherchance of one conceptual proposition being generated even withreduced activation levels (vs. a lower chance if only one or fewoptions are possible, in addition to reduced activation). We suggestit is unlikely that the performance of those LIFG patients who areimpaired on measures critically related to dynamic aphasia, suchas sentence generation from high frequency words, is underpinnedby another type of deficit.

Our findings are in keeping with previously reported dynamicaphasia case studies and the relevant lesion studies. First, dynamicaphasic patients who have been shown to have impaired word,phrase and sentence generation deficits when selection is required,tend to have lesions specifically involving the LIFG (Robinson etal., 1998, 2005) or more generally the left frontal region (Raymer,Rowland, Haley, & Crosson, 2002; Warren et al., 2003). They areinterpreted as due to problems of selection at the conceptualproposition level–in the conceptual preparation domain in Levelt’sapproach to language production.

Our findings also have some resemblance to a variety of studieson the lexical selection level. These include those of Thompson-Schill et al. (1998) who studied 4 patients with LIFG damage whowere specifically impaired in generating a single word when selec-tion from amongst competitors was required. Two further groupstudies investigated lexical selection in aphasic patients using a pic-ture naming paradigm. Schnur et al. (2005, 2009) provide evidencethat damage to the LIFG is associated with an increase in block-ing errors across picture naming cycles that they argue parallelsan increase in competition. Jefferies and Lambon Ralph (2006) andJefferies et al. (2007, 2008) similarly investigated picture namingas well as word-picture matching in aphasic patients and pro-posed that controlled executive processes, referred to as “selectinga word in naming or a picture in word-picture matching” (p. 1067,2007), are underpinned by both the posterior left prefrontal andtemporoparietal regions.

These second set of studies, however, deal with lexical selectionrather than higher-level selection between conceptual propo-sitions. Our findings provide evidence that only as far as thehigh-level conceptual proposition selection process is concernedit is the LIFG but not the temporoparietal region that is impor-

1 sychol

tpospeioas

do22taps2

660 G. Robinson et al. / Neurop

ant. Despite problems with naming our left temporal and posterioratients were intact on the critical condition for selection (andther conditions). Interestingly, Jefferies et al. (2007) report theiremantic refractory effects were weaker in two patients with tem-oroparietal infarcts. In terms of where these picture namingffects arise in the language generation process, Schnur et al. specif-cally related their findings to a deficit at the lexical selection stagef speech production. This is in contrast to our position as we wouldrgue that conceptual preparation selection occurs prior to lexicalelection and grammatical encoding (see above).

Within the neuroimaging literature the main processingemand accounts of the LIFG suggest it has a role in the retrievalf semantic information (Gabrieli et al., 1998; Wagner et al.,001) or subserves controlled semantic retrieval (Wagner et al.,001). Recently, a two-process account of the LIFG was proposed

hat distinguished between “a controlled retrieval process thatctivates goal-relevant knowledge in a top-down manner, and aost-retrieval selection process that resolves competition betweenimultaneously active representations” (p. 2885; Badre & Wagner,007). The post-retrieval selection process would fit with the selec-

ogia 48 (2010) 1652–1663

tion mechanism referred to in our approach. It has also beensuggested that the anterior portion of the LIFG subserves seman-tic processing whilst the posterior portion has been implicated inphonological and syntactic processing (e.g., Amunts et al., 2004;Paulesu et al., 1997; Poldrack et al., 1999). Our findings are equiv-ocal in this respect. In particular, four LIFG patients producedsemantic errors and one produced phonological errors. Of thesefive patients, four had LIFG lesions including both the anteriorand posterior portion and the one patient with only a posteriorlesion made semantic errors, contrary to what might have beenexpected.

Overall, for sentence and word generation from a singleword, there is strong convergence between lesion group studyfindings, the single case studies of dynamic aphasic patientsand neuroimaging data. This convergence across methodolo-

gies provides strong evidence for a role of the LIFG in ahighly specialised cognitive mechanism involved in propositionallanguage generation; namely, the high-level selection of concep-tual propositions from amongst competitors (sentence or wordlevel).

A

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G. Robinson et al. / Neuropsychologia 48 (2010) 1652–1663 1661

ppendix A.

Imaging, aetiology, lesion extent and chronicity within frontal (LIFG and Non-LIFG) and posterior patient groups.atient number Imaging: MRI/CT Aetiology Lesion extent: number of frontal areas Time post surgery (S) or event (E) in months∼rontal: LIFG

MRI Astrocytoma 8 0.10 (S)MRI Glioma 8 16.00 (S)CT Traumatic Brain Injury 2 1.00 (E)MRI Astrocytoma 8 36.20 (S)MRI Stroke 6 16.20 (E)MRI Lobectomy 9 96.50 (S)CT Meningioma 4 1.00 (S)MRI Meningioma 7 0.83 (S)MRI Glioma 2 0.17 (S)

0 MRI Stroke 5 11.10 (S)1 MRI Left Stroke 1 0.30 (E)2 MRI Glioma 4 0.00*= 12

rontal: Non-LIFG3 MRI Left Psuedotumour 4 4.00 (S)4 CT Left ACoA 1 9.57 (E)5 CT Left Glioma 1 11.20 (S)6 MRI Left Glioma 2 1.40 (S)7 MRI Left Astrocytoma 4 17.20 (S)8 MRI Left Astrocytoma 5 60.30 (S)9 CT Left ACoA 3 20.20 (E)0 MRI Left Glioma 1 0.47 (S)1 CT Medial Brain Abscess 5 0.33 (S)2 MRI Medial Meningioma 6 0.80 (S)3 MRI Medial Glioma 5 0.47 (S)4 MRI Medial ACoA 2 0.17 (S)5 MRI Medial Glioma 3 52.00 (S)6 CT Right Chronic Subdural Haematoma 4 67.00 (S)7 MRI Right Meningioma 9 181.00 (S)8 CT Right Meningioma 1 0.40 (S)9 MRI Right Stroke 4 14.00 (E)0 MRI Right Stroke 1 2.97 (E)1 CT Right Chronic Subdural Haematoma 4 0.67 (S)2 CT Right Meningioma 6 12.00 (S)3 MRI Right Glioma 2 15.00 (S)4 MRI Right Meningioma 7 5.83 (S)5 MRI Right Meningioma 8 52.60 (S)6 CT Right Meningioma 3 28.00 (S)7 CT Right Astrocytoma 4 0.17 (S)8 MRI Right Stroke 2 3.03 (E)9 CT Right Stroke 4 1.67 (E)0 CT Right Glioma 5 0.47 (S)1 MRI Right Meningioma 3 0.23 (S)2 MRI Right Meningioma 4 0.27 (S)3 MRI Right Glioma 1 0.15 (S)4 MRI Right Stroke 1 5.00 (E)5 MRI Right Meningioma 3 114.00 (S)6 MRI Right Glioma 1 42.00 (S)7 MRI Right Meningioma 5 24.00 (S)= 35

osterior8 MRI Left temporal glioma 0.73 (S)9 CT Left temporal abscess 3.20 (S)0 MRI Left temporal meningioma 3.00 (S)1 MRI Left temporal glioma 0.67 (S)2 MRI Left temporal stroke 42.60 (E)3 MRI Left temporal-parietal stroke 0.73 (E)4 MRI Left parietal glioma 0.23 (S)5 MRI Left parietal meningioma 21.20 (S)6 MRI Left parietal meningioma 0.13 (S)7 MRI Left parietal meningioma 0.40 (S)8 MRI Left parietal-occipital bleed 0.67 (E)9 MRI Left parietal glioma 0.17 (S)0 MRI Right temporal glioma 0.07 (S)1 MRI Right temporal glioma 0.10 (S)2 MRI Right temporal meningioma 12.70 (S)3 MRI Right temporal lobectomy for epilepsy 0.15 (S)

4 MRI Right parietal meningioma5 MRI Right parietal meningioma6 MRI Right parietal meningioma7 MRI Right parietal-occipital meningioma= 20

(∼) e.g., 1.00 = 30 days; (*) assessed prior to surgery.

0.13 (S)0.23 (S)2.00 (S)0.20 (S)

1

A

Htpcwmwfpthfrlmm

R

A

A

B

B

B

B

B

B

B

B

B

CC

D

D

D

G

G

G

H

H

I

I

662 G. Robinson et al. / Neuropsychologia 48 (2010) 1652–1663

ppendix B.

Experimental sentence generation stimuli.igh Frequency words Low Frequency words Proper Nouns

able thimble Hitlerlant bagpipe Eiffel Towerhildren claw Italyall helmet Mona Lisaan hockey Gandhiater kite South America

ace tutu Napoleonicture leotard George W Bushime pagoda Twin Towersistory monocle London

amily sporran Tony Blairoom sundial Afghanistanaw chopsticks Beatles

other trampoline David Beckhamoment shuttlecock Ireland

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