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Neurophysiological Correlates of Comprehending Emotional Meaning in Context

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Neurophysiological Correlates of Comprehending Emotional Meaning in Context Neurophysiological Correlates of Comprehending Emotional Meaning in Context Daphne J. Holt1, Spencer K. Lynn2, and Gina R. Kuperberg1,3 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/21/11/2245/1759801/jocn.2008.21151.pdf by guest on 18 May 2021 Abstract & Although the neurocognitive mechanisms of nonaffective and positive (relative to neutral) words was detected, with no language comprehension have been studied extensively, rela- differences found between N400 magnitudes to negative and tively less is known about how the emotional meaning of lan- positive words. Taken together, these results suggest that com- guage is processed. In this study, electrophysiological responses prehending the emotional meaning of words following a neutral to affectively positive, negative, and neutral words, presented context requires an initial semantic analysis that is relatively within nonconstraining, neutral contexts, were evaluated under more engaged for emotional than for nonemotional words, conditions of explicit evaluation of emotional content (Experi- whereas a later, more extended, attention-modulated process dis- ment 1) and passive reading (Experiment 2). In both experi- tinguishes the specific emotional valence (positive vs. negative) ments, a widely distributed Late Positivity was found to be larger of words. Thus, emotional processing networks within the brain to negative than to positive words (a ‘‘negativity bias’’). In addi- appear to exert a continuous influence, evident at several stages, tion, in Experiment 2, a small, posterior N400 effect to negative on the construction of the emotional meaning of language. & INTRODUCTION tic contextual relationship between an eliciting word During language comprehension, the final representation and its preceding context: the N400 (Kutas & Hillyard, of meaning that is generated is dependent on multiple 1980, 1984). The N400 is a centro-posteriorly distribut- neurocognitive processes that come into play at different ed, negative-going waveform that starts at approximately time points. The meaning of each incoming word is ini- 300 msec and peaks at approximately 400 msec after tially integrated with that of its preceding context and the onset of a critical word. The amplitude of this wave- with respect to preexisting knowledge, and then, under form is larger (more negative) to critical words that are some circumstances, additional cognitive processes are semantically unassociated (vs. associated) with preced- engaged to more fully evaluate the meaning constructed. ing single words in semantic priming paradigms (Bentin, However, the mechanisms underlying the construction of McCarthy, & Wood, 1985; Rugg, 1985) and that are incon- meaning of emotionally evocative language are poorly gruous (vs. congruous) with their preceding sentence con- understood. The present study used event-related poten- texts (Kutas & Hillyard, 1980, 1984) or global discourse tials (ERPs)—a direct index of on-line neural activity—to contexts (Van Berkum, Hagoort, & Brown, 1999). In addi- examine the neurocognitive processes underlying the tion to being evoked by frank semantic anomalies (Kutas comprehension of emotional language, both when par- & Hillyard, 1980), the amplitude of the N400 is larger to ticipants paid explicit attention to emotional content and plausible words that are unpredictable (vs. highly predict- under more passive reading conditions. Our focus was on able) with respect to their preceding context (Kutas & the modulation by emotion of two ERP components—the Hillyard, 1984), to implausible words that are categorically N400 and the Late Positivity. Below we review these two unrelated (vs. categorically related) to a predicted word components in relation to both the comprehension of (Federmeier & Kutas, 1999; Kutas & Hillyard, 1984), and language and emotional information. to words that are inconsistent (vs. consistent) with our knowledge of what is commonly encountered in the world (Hagoort, Hald, Bastiaansen, & Petersson, 2004; Kuperberg, Building Up Meaning during Language Comprehension Sitnikova, Caplan, & Holcomb, 2003). Taken together, The N400 and Semantic Memory this previous work suggests that the N400 reflects, at least It has been known since the early 1980s that there is in part, the process of directly mapping an evolving rep- a distinct neural measure that is sensitive to the seman- resentation of meaning on to stored knowledge, whether this be stored associations about what we know to be 1Massachusetts General Hospital, Boston, MA, 2McLean Hospi- true (Hagoort et al., 2004), what types of events we think tal, Belmont, MA, 3Tufts University, Medford, MA are likely to occur (Kuperberg et al., 2003), or stored D 2008 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 21:11, pp. 2245–2262 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.2008.21151 by guest on 28 September 2021 semantic associations (Van Petten, 1993) and categorical 2007). Studies examining patterns of evaluative ratings and featural relationships (Federmeier & Kutas, 1999) of words have found evidence for a structure of emo- between individual words—a process that has been tion knowledge that includes dimensions of valence, referred to, generally, as a semantic memory-based anal- arousal, and potency or dominance (Kissler, Assadollahi, ysis (Kuperberg, 2007; Kutas, Van Petten, & Kluender, & Herbert, 2006; Osgood, Suci, & Tannenbaum, 1957). 2006; Kutas & Federmeier, 2000). Because valence and arousal appear to account for much of the variance in these ratings, a two-dimensional model of affective meaning has been largely adopted (Feldman, Late Positivities in Language Processing 1995; Russell, 1980; Lang, 1979). These dimensions of In addition to a semantic memory-based analysis, under word meaning also apply to nonlinguistic representa- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/21/11/2245/1759801/jocn.2008.21151.pdf by guest on 18 May 2021 certain conditions, additional cognitive processes may be tions, such as pictures and sounds (Bradley, Codispoti, engaged in a further effort to integrate and evaluate a Cuthbert, & Lang, 2001; Bradley & Lang, 2000), sug- word with respect to its preceding context. This addition- gesting that they may be represented amodally within al analysis is often manifested by a centro-posteriorly dis- semantic memory. An additional source of evidence that tributed Late Positive component that onsets and peaks emotion concepts are stored and structured within se- at a later time point than the N400 and that can extend mantic memory comes from affective semantic priming until approximately 800 or 900 msec after stimulus onset. studies in which the processing of target words with The Late Positivity is evoked by words that violate the emotional meaning is facilitated by the presence of prime syntactic or thematic structure of their preceding context words of similar affective valence, and slowed by the (the P600) (Kuperberg, 2007; Hagoort, 1993; Osterhout presentation of words with a dissimilar valence (Bargh, & Holcomb, 1992), and is also seen in various other Chaiken, Raymond, & Hymes, 1996; Fazio, Sanbonmatsu, situations, such as during the comprehension of meta- Powell, & Kardes, 1986), although the precise mecha- phor (Coulson & Van Petten, 2002) and jokes (Coulson & nisms by which this occurs are debated (Spruyt, Hermans, Kutas, 2001). In all of these cases, a continued analysis De Houwer, Vandromme, & Eelen, 2007; Klinger, Burton, (or reanalysis) of the relationship between the eliciting & Pitts, 2000). stimulus and the context are required in order to recover Other studies have suggested that emotional infor- a full and accurate representation of meaning. mationisrepresentedinthebraininadistributed, The degree to which the Late Positivity reflects partic- ‘‘embodied’’ manner—the meaning of emotional infor- ular linguistic processes (Kuperberg, 2007; Osterhout & mation is retrieved via a simulation of the emotionally Hagoort, 1999) or more general processes (Kolk & evocative stimulus or overall experience (Niedenthal, Chwilla, 2007; Coulson, King, & Kutas, 1998) is debated. 2007; Glenberg, Havas, Becker, & Rinck, 2005). Evidence Late Positivities have often been viewed as part of the in support of this model comes from studies show- P300 family of ERP components that are modulated by the ing that mood and bodily states can ‘‘prime’’ the com- subjective probability of the eliciting stimuli (with more prehension (Glenberg et al., 2005) and classification positive amplitudes with greater task relevance) and index (Niedenthal, Halberstadt, & Innes-Ker, 1999) of repre- the degree to which a working model of the environment sentations that are emotionally congruent with the body requires updating (Donchin & Coles, 1988). Nonetheless, or mood state. For example, in one study, reading times although the Late Positivity, like the P300, is modulated by of emotionally laden sentences were faster when partici- task and, in some situations, by the probability of the pants were induced to have mood-congruent (vs. mood- eliciting stimulus, it can be present and modulated even incongruent) facial expressions without their awareness during passive reading and listening, without additional (Havas, Glenberg, & Rinck, 2007), suggesting that such task requirements, suggesting that the processes it re- emotion knowledge can rapidly influence on-line lan- flects can be inherent to naturalistic on-line comprehen- guage comprehension.
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