Right semantic modulation of early MEG components during ambiguity resolution
Graphical abstract
Introduction
It is widely believed that for over 90% of the population both language and handedness are lateralized to the left hemisphere (LH; Tzourio-Mazoyer et al., 2010). A major evidence for the laterality of language is the fact that damage to LH language regions often leads to aphasia while RH damage causes aphasia only in rare cases (Faglia et al., 1990). Therefore, the RH is generally considered to play a minor role in simple language processing. However, the RH is hypothesized to participate in language processing along with the dominant left hemisphere in situations with complex content such as a joke or an indirect request (Gardner and Brownell, 1986, Gardner et al., 1975, Zaidel, 2001). Gazzaniga (1983) suggested that a possible role of the RH is to assist the left hemisphere (LH) by validating one out of few possible interpretations. The general aim of this work is to explore the regions and time-course of activity of RH language function. To that purpose, we chose to focus on a task involving ambiguous words (bank) with dominant (money) and subordinate associations (river). This allows manipulating the complexity levels using relatively simple stimuli. We expected to measure increased activity over the RH when dealing with subordinate, compared to the dominant associations, and planned to estimate the timing and location of the increased activity.
Some ambiguous words are biased to one dominant meaning (Burgess and Simpson, 1988) which is their frequent (Rayner and Frazier, 1989) or salient (Giora, 2007) meaning. The other meaning is called subordinate. When one reads a sentence containing a biased ambiguous word such as “I went to the bank and it was closed” the word bank is interpreted without difficulty because its dominant meaning (financial institution), is relevant to the sentential context. The sentence “I went to the bank and the boat wasn't there” introduces a difficulty because the dominant meaning is irrelevant. When one reads the word boat (disambiguating clue) the reader realizes that bank more probably stands for a river bank which is its subordinate, or less frequent, meaning. It has been shown in gaze studies (Rayner and Frazier, 1989) that special effort in disambiguation (of biased words) is required for subordinate meanings while dominant meanings are processed similarly to unambiguous words.
Jung-Beeman's model (2005) for fine and coarse semantic coding advocates that biased ambiguous words activate their subordinate, as well as their dominant, meanings in the right homologue of Wernicke's area. As soon as a subsequent subordinate association word appears, the right anterior temporal lobe attempts to integrate its meaning with the pre-activated meanings of the ambiguous word. This process is followed by the selection of the relevant concept in the right inferior frontal gyrus (IFG; see also at Thompson-Schill et al., 1997). Federmeier and Kutas (1999) also suggested that the RH contributes to ambiguity resolution by integrating subordinate meanings to context (see also the PARLO framework, Federmeier, 2007), whereas the LH specializes in prediction. Thus, according to both models subordinate meanings should activate RH more than dominant meanings.
Many studies on ambiguity processing have used tasks which did not require explicit ambiguity resolution (e.g., Bilenko et al., 2009, Burgess and Simpson, 1988, Copland et al., 2007, Grindrod and Baum, 2003, Klepousniotou, 2002, Peleg and Eviatar, 2008). However, since our purpose was to explore the neuronal correlates of left and right semantic processing the current study employed explicit semantic processing of word pairs consisting of biased ambiguous words coupled with disambiguation words or unrelated ones. The task was to indicate by button press whether the second word was related to the first or not. Therefore, in order to respond correctly subjects had to resolve the ambiguity. Previous language laterality studies with explicit semantic processing of ambiguous words have used visual hemifield presentation (Faust and Lavidor, 2003, Harpaz and Lavidor, 2012), transcranial magnetic stimulation location (Harpaz et al., 2009), fMRI activation (Zempleni et al., 2007) and lesion site (Gardner and Brownell, 1986, Zaidel et al., 2002). These studies generally concluded that the RH participates in ambiguity resolution. However, the methods used in these studies do not allow fine spatio-temporal resolution and therefore it is impossible to deduce from these studies when each brain region was active. The time course of brain activity during word reading has been examined using EEG/MEG measures that have adequate temporal resolution. It is commonly viewed that the orthographic decoding is manifested early on in the N170 component (Bentin et al., 1999, Cohen et al., 2000). There is also agreement that the N400 (M350) component reflects semantic processing (see review: Pammer, 2009). However, some studies (Dell'Acqua et al., 2007, Pulvermüller et al., 2001, Sereno et al., 1998) have found evidence for semantic processing less than 200 ms after word onset. An EEG study of lexical ambiguity that used the N400 amplitude as a metric for semantic processing found evidence for hemispheric asymmetry in ambiguous word processing at this stage (Atchley and Kwasny, 2003). Brain responses to related and unrelated ambiguous words differed when presented to the LH, but not when presented to the RH. This suggested that the very broad representation of an ambiguous word in the RH does not generate semantic expectations (thus no N400 difference). In contrast, in the LH unrelated words elicited higher N400 amplitude than the dominant related words. A differential response was found in the LH also for subordinate meanings, although it was significantly delayed. The insensitivity of the N400 component to subordinate meanings in left visual field trials may imply that the RH did not contribute to semantic processing. This stresses the importance of finding the conditions in which the RH does contribute.
The current work aimed to define the time-course of RH activity during lexical ambiguity resolution. In order to maximize the involvement of the RH in the task, we measured the brain activity elicited by subordinate associations of biased ambiguous words and compared it with the responses to dominant associations. The stimulus onset asynchrony was set over 750 ms to allow the meanings of the ambiguous words to be activated in the two hemispheres before the display of the disambiguation clue (Burgess and Simpson, 1988, Frost and Bentin, 1992). The meaning (dominant vs. subordinate) was manipulated between blocks, since it had been found that the blocked design facilitates hemispheric expertise for ambiguity processing, possibly through conditioning the brain to use the expert hemisphere according to block meaning (Harpaz and Lavidor, 2012). We employed a semantic decision task to ensure that the correct meaning of the ambiguous words was processed. Trials with words unrelated to the ambiguous word served mainly as filler items and were necessary for setting the rate of positive answers at 50%, thus avoiding response bias. The contrast of interest was the difference in brain activity elicited by subordinate relative to dominant meaning words. We predicted that the comparison between subordinate and dominant related associations would reveal greater activity in RH language regions. Furthermore, we examined whether the conditions would help reveal RH contribution at early stages of processing.
Section snippets
Participants
Twenty five students (4 male, mean age 29.6) participated after giving informed consent. All were right-handed (scoring at least 90 on the Edinburgh Handedness inventory; Oldfield, 1971) native Hebrew speakers. Their sight was normal or corrected to normal.
Design
A factorial 2 × 2 design was applied, with meaning (dominant, subordinate) and relatedness (related, unrelated) as within subject factors. The unrelated trials were used in this study only as filler trials to allow the semantic task and were
Behavior
Repeated measures ANOVA was applied for the RT and error rates with meaning (dominant, subordinate) and relatedness (related, unrelated) as within subject factors. The accuracy rates revealed a significant interaction (F(1,24) = 13.24, MSW = 0.022, p < 0.005). A Bonferroni post hoc test revealed that the interaction was due to higher error rates for subordinate-related (19%) compared to dominant-related (11%), subordinate-unrelated (10%) and dominant-unrelated (8%; all with p < 0.001).
For the RT, the
Main findings
The current study employed MEG to explore the spatio-temporal aspects of lexical ambiguity resolution and in particular, the involvement of the RH. A significant increase in activity for unrelated and related target words in the subordinate block was measured over the RH around 170 ms from target onset. This increased activity was localized by beamforming to the right perisylvian area, including the homologous regions of Broca and Wernicke.
Behavior
The behavioral results show that the subordinate related
Conclusion
The current study elucidates the timeline of RH involvement in ambiguity resolution. It reveals that the RH language regions increase their activity between 150 and 235 ms from the onset of a disambiguating word for subordinate meaning processing. This and future similar studies should be used for improving existing models of reading and language processing to specify which brain regions are active in the two hemispheres and their time course of activity. As far as we know, no such models exist
Acknowledgment
This work was supported in part by the Israeli Center of Research Excellence (I-CORE) in Cognition (I-CORE Program 51/11).
Conflict of interest statementThe authors declare no conflict of interest for the content of this article.
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