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Common and Distinct Neural Substrates for Pragmatic, Semantic, and Syntactic Processing of Spoken Sentences: an Fmri Study

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Common and Distinct Neural Substrates for Pragmatic, Semantic, and Syntactic Processing of Spoken Sentences: an Fmri Study Common and Distinct Neural Substrates for Pragmatic, Semantic, and Syntactic Processing of Spoken Sentences: An fMRI Study G.R.Kuperberg and P.K.McGuire Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/12/2/321/1758711/089892900562138.pdf by guest on 18 May 2021 Institute of Psychiatry, London E.T.Bullmore Institute of Psychiatry, London and the University of Cambridge M.J.Brammer, S.Rabe-Hesketh, I.C.Wright, D.J.Lythgoe, S.C.R.Williams, and A.S.David Institute of Psychiatry, London Abstract & Extracting meaning from speech requires the use of difference between conditions in activation of the left-super- pragmatic, semantic, and syntactic information. A central ior-temporal gyrus for the pragmatic experiment than the question is:Does the processing of these different types of semantic/syntactic experiments; (2) a greater difference be- linguistic information have common or distinct neuroanatomi- tween conditions in activation of the right-superior and middle- cal substrates? We addressed this issue using functional temporal gyrus in the semantic experiment than in the syntactic magnetic resonance imaging (fMRI) to measure neural activity experiment; and (3) no regions activated to a greater degree in when subjects listened to spoken normal sentences contrasted the syntactic experiment than in the semantic experiment. with sentences that had either (A) pragmatical, (B) semantic These data show that, while left- and right-superior-temporal (selection restriction), or (C) syntactic (subcategorical) viola- regions may be differentially involved in processing pragmatic tions sentences. All three contrasts revealed robust activation of and lexico-semantic information within sentences, the left- the left-inferior-temporal/fusiform gyrus. Activity in this area inferior-temporal/fusiform gyrus is involved in processing all was also observed in a combined analysis of all three three types of linguistic information. We suggest that this experiments, suggesting that it was modulated by all three region may play a key role in using pragmatic, semantic types of linguistic violation. Planned statistical comparisons (selection restriction), and subcategorical information to between the three experiments revealed (1) a greater construct a higher representation of meaning of sentences. & INTRODUCTION Does the processing of pragmatic, semantic, and syntac- As we listen to speech, we continually use different tic information have distinct neuroanatomical correlates, forms of linguistic informationÐsemantic (the meaning or do they share a common neural substrate? The of words), syntactic (grammatical) and pragmatic (our evidence for autonomy at the neuroanatomical level is understanding of the world)Ðto build up an overall conflicting. A number of neuropsychological and elec- representation of meaning (Kintsch, 1988; Johnson- trophysiological dissociations between semantic, prag- Laird, 1987). As these different forms of linguistic in- matic, and syntactic processing have been described, formation have different rules and representations, they yet, there is also evidence that some of the same brain are generally acknowledged to be independent of one regions may support processing of these different forms another. However, a fundamental question is whether of linguistic information. this linguistic autonomy is paralleled by a processing autonomy. This question relates both to the stage at Semantic vs.Syntactic Processing which these linguistic processes influence each other, as well as to their localization in the brain. In this study, we Converging evidence from neuropsychological (Rapcsak address the issue of localization. We ask the question: & Rubens, 1994; Hodges, Patterson, Oxbury, & Funnell, D 2000 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 12:2, pp. 321±341 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892900562138 by guest on 23 September 2021 1992; Graff-Radford et al., 1990; Kempler et al., 1990; tionÐthe argument structure or subcategorization Alexander, Hiltbrunner, & Fischer, 1989; Pietrini et al., frameÐplaces additional constraints on the object 1988; Poeck & Luzzatti, 1988; Sartori & Job, 1988; De noun. Thus, in a semantically violated sentence such Renzi, Zambolin, & Crisi, 1987; Warrington & Shallice, as ``the man drank the guitar'' (see Table 1), the 1984), event-related potential (ERP) (Nobre & McCarthy, semantic selection restriction properties of the verb 1995), and functional imaging (Damasio, Grabowski, ``drank'' are incongruous with the object noun ``guitar'' Tranel, Hichwa, & Damasio, 1996; Martin, Wiggs, Un- despite the two words being syntactically compatible. gerleider, & Haxby, 1996; Vandenberghe, Price, Wise, In contrast, the sentence ``the young man slept the Josephs, & Frackowiak, 1996; Demonet et al., 1992b; guitar'' is violated both semantically and syntactically Goldenberg, Podreka, Steiner, & Willmes, 1987) studies (subcategorically), because the verb ``slept'' cannot take Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/12/2/321/1758711/089892900562138.pdf by guest on 18 May 2021 suggests that left-sided inferior-temporal-cortical regions a direct object (which should be preceded by a pre- play a crucial role in lexico-semantic processing. On the position). other hand, the study of agrammatic aphasic patients Whether subcategorical syntactic processing can be has implicated left-anterior-inferior-frontal regions in dissociated from semantic processing within sentences building up the syntactic structure of sentences (Frazier is controversial. From a linguistic perspective, the syn- & Friederici, 1991; Caplan, Baker, & Dehaut, 1985; tactic aspect of a verb (specified on the subcategoriza- Caramazza & Zurif, 1976). This is supported by recent tion frame) can be seen as a projection of some of its functional imaging investigations (Caplan, Alpert, & semantic features (Chomsky, 1981; Bresnan, 1979; Jack- Waters, 1998; Just, Carpenter, Keller, Eddy, & Thulborn, endoff, 1978). By this account, the meaning of a verb 1996; Stromswold, Caplan, Alpert, & Rauch, 1996). and its syntactic aspects are tightly intertwined, and However, most of the studies exploring syntactic might, therefore, be subserved by the same brain net- processing have focused on the parsing of complex works. On the other hand, Ostrin and Tyler (1995) have sentences; the question of whether the same brain described a patient (JG) who cannot process subcate- regions mediate semantic and syntactic processing gorization information, but who processes lexical±se- within simple sentences has been relatively unexplored. mantic information normally. Moreover, ERP waveforms This question is critical, as a central theory of language elicited by subcategorization violations show a more processing holds that sentence parsing is guided by anterior scalp-distribution than those elicited by purely lexical information held within the verb (reviewed by semantic violations (Friederici, 1995; Rosler, Friederici, Garrett, 1992; Levelt, 1989). Verbs contain both seman- Putz, & Hahne, 1993), suggesting that the two processes tic and syntactic information. The syntactic informa- can be spatially dissociated. Table 1. Types of Linguistic Violations Example illustrating how the relationship between verb and object noun can be varied to change meaning of Example used in Linguistic violation Explanation whole sentencea current study None Baseline condition against which the ``The young man grabbed ``The boy counted the other conditions are evaluated the guitar'' ducks'' Pragmatic Sentence is pragmatically implausi- ``The young man buried ``The woman painted (Experiment A) ble with respect to our knowledge the guitar'' the insect'' of real world events. Semantic (selection restriction) Semantic properties of verbs are ``The young man drank ``My mother ironed a (Experiment B) incompatible with the semantic the guitar'' kiss'' properties of object nouns. Syntactic (subcategorical violation) Intransitive verbs are chosen so that ``The young man slept the ``His father chattered (Experiment C) a noun in the direct object posi- guitar'' the umbrella'' tion cannot follow them. Word-strings Word-strings with no syntactic or ``young the the slept man ``money the the client semantic structure guitar'' washed'' aThis example is adapted from that given in Spoken Language Comprehension (p. 107) by L.K. Tyler, 1992, London:MIT Press. 322 Journal of Cognitive Neuroscience Volume 12, Number 2 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892900562138 by guest on 23 September 2021 Pragmatic vs.Lexico-Semantic and Subcategori- brain areas are thought to be specifically dedicated to zation Processing processing at the sentential vs. lexical level. This assump- tion may, to some extent, be justified. For example, ``Pragmatic processing'' is a rather loosely defined term, some studies suggest that anterior-inferior-temporal re- and has been used to refer to a wide range of cognitive gions are specifically engaged in higher-level sentential processes, many operating upon narrative and dis- processing (Mazoyer et al., 1993). However, the investi- course-level material such as nonliteral language, stories, gation of neural correlates of specific levels of sentence jokes, and conversations. The study of right-brain-da- processing (i.e., pragmatic, semantic, syntactic) de- maged patients suggests that some of these operations mands alternative approaches. are subserved by the right hemisphere (Joanette
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