Special issue: Research reportLexical ambiguity resolution in Wernicke's area and its right homologue
Introduction
More than a century ago, Broca (1865) and Wernicke (1874) argued that language is mainly a left hemisphere (LH) function. Their clinical findings showed that the LH but not the right hemisphere (RH) lesions caused severe language impairments such as the inability to understand or generate speech. More recently it has been shown that damage to the RH in the homologue areas usually results in subtle language deficits such as impaired comprehension of jokes (Gardner et al., 1975) or metaphors (Winner and Gardner, 1977).
Numerous models have been put forward to account for hemispheric differences (Dien, 2008) with some overlap between theories. In the current study, we define hemispheric differences in semantic processing as characterized by a tendency of the LH to process stimuli analytically (Levy-Agresti and Sperry, 1968) when dealing with routine (Goldberg and Costa, 1981), frequent (Sergent, 1982) and salient meanings (Giora, 2007). By contrast, the RH processes in a Gestalt mode (Levy-Agresti and Sperry, 1968) and may perceive novel (Goldberg and Costa, 1981), infrequent (Sergent, 1982) and non-salient (Giora, 2007) aspects of language. Jung-Beeman (2005) suggested that in the RH, widespread groups of interconnected neurons are activated by lingual stimuli, whereas such stimuli activate a more restricted group of neurons in the LH. This restricted activation enables fine encoding in the LH which is appropriate when the precise, frequent meaning of a term is required. In a complementary fashion, the coarser processing in the RH may be useful when words are remotely associated (Giora, 2007). However the evidence to support the fine-coarse coding theory (Jung-Beeman, 2005) is correlational at best since it is drawn from the few existing functional Magnetic Resonance Imaging (fMRI) studies.
As a test case to reveal potential hemispheric differences in semantic processing we studied ambiguous words that have a subordinate meaning in addition to their dominant, frequent meaning. Based on brain lesion observations (Gardner and Brownell, 1986) and divided visual field studies with healthy participants (Burgess and Simpson, 1988) it has been suggested that the RH has a special role in lexical ambiguity resolution. However, these research methods were unable to identify the specific region within the RH that participates in the process.
In contrast, today's imaging studies can contribute to finer localization of RH language centers. Rodd et al. (2005) contrasted auditory sentences containing ambiguous words (The shell was fired towards the tank) with matched sentences that did not contain ambiguous words. Although the study did not distinguish between subordinate and dominant meanings, the results showed that along with Broca's region and Wernicke's area (in the LH), the right homologue of Broca's region (the triangular and opercular parts of the right inferior frontal gyrus) was also activated by ambiguity. Since activation in the regions of interest was the dependent variable, it is impossible to determine whether the ambiguous stimuli caused RH activity which resulted in comprehension, or whether the ambiguous stimuli caused RH activity but comprehension was achieved independently by another neuronal mechanism. Electro-EncephaloGraphy (EEG) studies have revealed that ambiguous word processing modulates the N400 ERP component under certain contextual conditions. Sitnikova et al. (2003) showed that the N400 component is more negative for an incongruent context of ambiguous words than a congruent context (see also Titone and Salisbury, 2004). This interaction was found for healthy subjects, and not patients with schizophrenia, a disease known to cause impaired processing of ambiguous words (Chapman et al., 1976). While these studies are informative as to the timing of neuronal processes, they cannot establish clear cut causal inferences regarding the role of the neuronal generator of the N400 component and the observed behavior, or shed light on the locus of the function.
Transcranial Magnetic Stimulation (TMS) has been used to locate language brain centers in simple tasks such as picture naming that do not normally call for RH involvement, similar to intraoperative methods which are used to prevent postoperative aphasia (Duffau et al., 2002, Eisner et al., 1996, Herholz et al., 1997, Ojemann, 1979, Ojemann et al., 1989, Rutten et al., 2002).
Two noninvasive TMS procedures have been used to assess the functionality of Wernicke's area. In one case, high frequency (20 Hz) stimulation decreased latency when applied during a naming task immediately before each trial (Mottaghy et al., 1999, Sparing et al., 2001). By contrast a 10-min low frequency (1 Hz) TMS train applied prior to the task (picture–name verification) resulted in inhibition (Drager et al., 2004, Flöel et al., 2000, Knecht et al., 2002). This suggests that Wernicke's region is enhanced by event-related high frequency TMS delivered during a behavioral experiment, and inhibited by offline low frequency TMS. Note that the TMS effect depends on location, task, intensity and frequency (Bestmann, 2008). Repetitive high frequency protocols may result in language inhibition if applied over different brain regions (e.g., Stewart et al., 2001), and similarly, low frequency offline protocols may yield a facilitation of language processing (Drager et al., 2004).
Both of these TMS protocols can be used to explore the causal role of brain regions. If language function is indifferent to neuronal activity in any brain region, then neither excitation nor inhibition of neurons in that region should alter behavior. Inhibitory and excitatory TMS effects can be thought of as higher and lower thresholds for neuronal activity in the stimulated region; neuronal input which normally causes neurons to fire will not suffice if the threshold was elevated by inhibitory TMS, whereas weak neuronal input may result in action potentials if the threshold was lowered by excitatory TMS. We chose an event-related design to explore the spatial and temporal characteristics of semantic processing. Following previous studies with similar protocols, we predicted facilitation following CP5/CP6 high frequency event-related stimulation.
We used a semantic decision task (Faust and Lavidor, 2003) where participants were asked to decide whether an ambiguous word was related or not to a subsequent word. The following word could be related to the dominant or subordinate meaning of the ambiguous word or not related at all.
Section snippets
Participants
Six female and five male students with no history of neurological illness participated after giving their informed consent. All were right handed (scoring at least 90 on the Edinburgh Handedness inventory; Oldfield, 1971) and native Hebrew speakers. Their sight was normal or corrected to normal, and their age ranged from 20 to 36 years. They received a fee equivalent to $ 40 for participating in the two-hour experiment.
Design
A factorial 2 × 3 × 2 design was applied, with BLOCK MEANING (dominant,
Results
Repeated measure ANOVAs were run separately for correct RT and accuracy, with BLOCK MEANING (dominant, subordinate), RELATEDNESS (related, unrelated) and TMS site (CP5, Cz, CP6) as within subject factors.
Discussion
The aim of the current study was to explore the involvement of the right homologue of Wernicke's area in the processing of subordinate meanings of ambiguous words. It has been claimed that the LH and RH focus on processing the dominant and subordinate meanings of ambiguous words, respectively, however a causal relationship between the hemispheres and meaning types could not be established with certainty. We used TMS to demonstrate causal links between cortical areas and cognitive functions.
Acknowledgments
This study was supported by grant no. 474/06 from the Israel Science Foundation and by a start-up grant by the European Research Council awarded to ML.
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