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The Response of Left Temporal Cortex to Sentences

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The Response of Left Temporal Cortex to Sentences The Response of Left Temporal Cortex to Sentences R. Vandenberghe1, A. C. Nobre2, and C. J. Price3 Abstract Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/14/4/550/1757525/08989290260045800.pdf by guest on 18 May 2021 & The meaning of a sentence differs from the sum of the response occurred in the left anterior superior temporal meanings of its constituents. Left anterior temporal cortex sulcus and the left posterior middle temporal gyrus. A subset responds to sentences more strongly than to unconnected of voxels within the left anterior temporal pole responded words. We hypothesized that the anterior temporal response more to semantically random sentences and their scrambled to sentences is due to this difference in meaning (composi- versions than to normal sentences and the corresponding tional semantics). Using positron emission tomography scrambled versions (main effect of semantic randomness). (PET), we studied four experimental conditions (2 Â 2 Finally, the grammatical and the semantic factor interacted in factorial design): In one condition, subjects read normal a subset of voxels within the anterior temporal pole: Activity sentences. In a second condition, they read grammatically was higher when subjects read normal sentences compared correct sentences containing numerous semantic violations to their scrambled versions but not for semantically random (semantically random sentences). In a third condition, we sentences compared to their corresponding scrambled scrambled the word order within the normal sentences, and, versions. The effects of grammar and meaning and, most in a fourth condition, the word order was scrambled within importantly, the interaction between grammatical and seman- the semantically random sentences. The left anterior tempo- tic factors are compatible with the hypothesis that the left ral pole responded strongly to sentences compared to anterior temporal pole contributes to the composition of scrambled versions of sentences. A similar although weaker sentence meaning. & INTRODUCTION et al., 1996). In the current study, we tried to determine By combining words into sentences, we can communi- which brain regions are involved in the composition of cate an unlimited variety of experiences and ideas. The sentence meaning from a syntactic combination of meaning of a sentence is a function of the individual meaningful words (Caplan, 1992; Taraban and McClel- meanings of its constituents and also of the way that land, 1990; Chomsky, 1986). they are syntactically combined (Partee, 1995). Composi- One candidate region is the left anterior temporal tional semantics refers to this difference in meaning pole. Left anterior temporal blood flow increases when between a sentence and an unstructured sequence of subjects listen to grammatically structured sequences of words (Fodor, 1995; Partee, 1995). pseudowords in comparison to a resting control con- Previous neuroimaging studies have defined the neu- dition but not when they listen to a list of unconnected ral substrate for syntactic operations by contrasting words (Mazoyer et al., 1993). It also increases when different types of sentences. They compared, for in- subjects read sentences compared to lists of uncon- stance, sentences with embedded clauses and with nected words (Stowe et al., 1998; Bottini et al., 1994), right-branching clauses (Stromswold, Caplan, Alpert, & nonwords (Bavelier et al., 1997), and fixation or Tamil Rauch, 1996), sentences with cleft-object and with cleft- pseudocharacters (Chee et al., 1999). This is surprising: subject phrases (Caplan, Alpert, & Waters, 1999) or Focal lesions of anterior temporal cortex can give rise to sentences of increasing complexity (Just, Carpenter, naming (Saykin et al., 1995; Hermann, Wyler, Somes, & Keller, Eddy, & Thulborn, 1996). In agreement with Clement, 1994; Devinsky, Perrine, Llinas, Luciano, & patient lesion studies (Zurif, Swinney, Prather, Solomon, Dogali, 1993) or semantic deficits (for review, see Saffran & Bushell, 1993; Caplan, 1992; Mesulam, 1990; Schwartz, & Sholl, 1999) but, to our knowledge, they do not lead Saffran, & Marin, 1980), these experiments successfully to clinically obvious sentence comprehension deficits. implicated the left frontal operculum in processing Recent evidence has implicated the left anterior tempo- syntax (Caplan et al., 1999; Just et al., 1996; Stromswold ral cortex in the processing of meaning. Left anterior temporal cortex is activated during lexical–semantic tasks where subjects have to retrieve proper names 1University Hospital Gasthuisberg, Leuven, 2Oxford Uni- (Gorno-Tempini et al., 1998; Damasio, Grabowski, Tranel, versity, 3University College London Hichwa, & Damasio, 1996) or where they actively D 2002 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 14:4, pp. 550–560 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/08989290260045800 by guest on 26 September 2021 compare the meanings of words or pictures (Vanden- would be higher when subjects read sentences in com- berghe, Price, Wise, Josephs, & Frackowiak, 1996). parison to scrambled word sequences (Mazoyer et al., Word-related responses in anterior temporal cortex 1993). Second, we expected that activity would be high- are affected by the semantic context provided by a er when the open class words were chosen randomly word list (Mummery, Shallice, & Price, 1999; Nobre, within a sentence or a word sequence (Nobre et al., Allison, & McCarthy, 1994). We hypothesized that the 1994). Finally, and most critically, we predicted that the anterior temporal response to sentences is related to effect of grammatical structure would depend upon the the composition of sentence meaning rather than to semantic content of the constituent words. syntactic operations in themselves. At least two previous studies (Ni et al., 2000; Dapretto Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/14/4/550/1757525/08989290260045800.pdf by guest on 18 May 2021 & Bookheimer, 1999) examined the anatomical relation- RESULTS ship between semantic and syntactic processing. Both The final image smoothness estimate was 9.2 Â 9.4 Â studies used fMRI, a technique that is less sensitive to 3 changes occurring in the anterior temporal pole (Devlin 15.0 mm . The search volume extended from z = À40 et al., 2000). One study compared between sentences mm to z = +68 mm. containing either a syntactic or a semantic anomaly (Ni et al., 2000). Syntactic anomalies activated the left Behavioral Data inferior frontal gyrus compared to semantic anomalies while the opposite was found in the left posterior Behavioral data from five of the positron emission temporal cortex (Ni et al., 2000). In a second study, tomography (PET) subjects were pooled with those subjects made a same–different judgement about the obtained from 10 additional subjects who did not under- meaning of sentences that either differed by the mean- go scanning. These subjects participated in an event- ing of one open class item or by their syntactic structure related potential version of the study where exactly (Dapretto & Bookheimer, 1999). Segregation was found identical materials were used. No data of the remaining in the left inferior frontal gyrus: Activity in Brodmann’s five PET subjects were available due to technical failure. area (BA) 47 was higher when sentences differed by one A repeated-measures 2 Â 2 factorial ANOVA was per- open class item while activity in BA44/45 was higher formed using grammatical structure and semantic ran- when sentences differed by their syntactic structure domness as factors. The behavioral measure was the (Dapretto & Bookheimer, 1999). The semantic condi- target detection response time. A target consisted of the tion in the study by Dapretto and Bookheimer (1999) repetition of two identical words within the visually involved a comparison between the meaning of lexical presented word series. There were no significant main items embedded in sentences. In contrast, we deter- effects. A significant interaction effect was found: Sub- mined which regions are involved in composing the jects responded significantly more slowly when they meaning of a sentence. read semantically random sentences (see Appendix: In this experiment, subjects read two types of sen- sequences of type Gram+SemÀ) compared to the cor- tences: normal sentences and grammatically correct responding scrambled versions (see Appendix: sequen- sentences containing numerous semantic violations ces of type GramÀSemÀ) but not when they read normal (semantically random sentences). The latter type of sentences (see Appendix: sequences of type Gram+ sentences conveyed a message that did not in any way Sem+) compared to the corresponding scrambled ver- correspond to potential real-life events. Nevertheless, sions (see Appendix: sequences of type GramÀSem+) both types of sentences could be written out formally as [F(2,460) = 4.2, p < .01] (Table 1). The behavioral data a sentence tree (Chomsky, 1986) indicating the subject, are in agreement with psychophysical studies indicating theverb,theobject,andsoforth.Foreachofthe that sentence context affects performance of tasks sentences, there was a corresponding scrambled ver- that are directed at the single-word processing level sion. We predicted that left anterior temporal activity (Marslen-Wilson & Tyler, 1980). Table 1. Behavioral Data Gram+ Sem+ GramÀSem+ Gram+ SemÀ GramÀSemÀ Gram+Ctrl GramÀCtrl RT (msec) 609 (170) 595 (214) 630 (215) 568 (144) 571 (136) 625 (182) False alarms
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