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Using event-related potentials to examine hemispheric differences in semantic processing
Brain and Cognition 53 (2003) 133–138 www.elsevier.com/locate/b&c
Using event-related potentials to examine hemispheric differences in semantic processing Ruth Ann Atchley and Kristin M. Kwasny University of Kansas, Lawrence, KS 66045, USA Accepted 7 May 2003
Abstract Event-related potentials (ERPs) were used as the dependent measure in a divided visual field study examining the processing of lexically ambiguous words in the cerebral hemispheres. The goal was to determine if the N400 ERP component is sensitive measure of hemispheric differences in semantic processing. ERP waveforms were examined for lateralized target words that were related to either the dominant (MONEY) or subordinate (RIVER) meanings of ambiguous words (BANK). These waveforms were compared to trials where the prime-target pairs were unrelated. Reliable N400s, reflecting a significant difference between related and unrelated trials, were seen when targets were presented to the right visual field/left hemisphere. However, there were no N400s observed for either the dominant or subordinate conditions when targets were presented to the left visual field/right hemisphere. Ó 2003 Elsevier Inc. All rights reserved.
1. Introduction Divided visual field (DVF) techniques have effectively been used as an method for examining hemispheric differences in lexical and semantic processing and have resulted in the development of a number of interesting models that postulate that both cerebral hemispheres contribute to language comprehension (see Beeman & Chiarello, 1998 for a review). The current study represents an important extension of this research in that both DVF stimulus presentation and event-related potentials (ERPs) are employed as dependent measures. Traditionally, behavioral dependent measures (such as naming or lexical decision) have been used in DVF studies and in particular the magnitude of priming (or the difference in reaction time or accuracy between related and unrelated trials) is commonly examined. Very little research has been done that uses ERPs to examine lateralized semantic processing (Federmeier & Kutas, 1999; McCarthy & Nobre, 1993; Swaab, Baynes, & Knight, 1998). The combination of DVF stimulus presentation and electrophysiological measurement will significantly contribute to the current literature because it provides information that cannot be gained with either behavioral measures alone or with electrophysiological 0278-2626/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved. doi:10.1016/S0278-2626(03)00095-2
measures using central visual field stimulus presentation. First, ERPs provide insight into the time course of language comprehension because they can provide data that reflect processing at each millisecond of the comprehension process (see Kutas & Van Petten, 1994). In contrast, behavioral measures reflect the summation of all the steps that elapse prior to the language taskÕs behavioral response. Regarding issues of cerebral lateralization, it is hard to draw conclusions regarding localization of function when considering ERP data because of the inverse problem inherent in most ERP research (McCarthy & Wood, 1985). We can avoid making potentially problematic assumptions based on conclusions drawn from the scalp distribution of the ERP waveforms by employing a DVF presentation of the targets. Lateralized presentation of stimuli leads to robust and reliable differences in word processing when response time and response accuracy are measured across a number of language tasks (Beeman & Chiarello, 1998). Therefore, it is reasonable to assume that this presentation technique should also influence ERP components in a way that should reflect hemispheric differences in language processing. One of the major goals of the current research was to determine if this assumption is well founded; to determine if ERP
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components are sensitive to hemispheric difference in language processing. One ERP component, referred to as the N400, is particularly sensitive to the semantic aspects of experimental stimuli and the magnitude of this waveform seems to be a reflection of the semantic compatibility between sequentially presented words (Kutus & Van Petten, 1994; Kutas, 1993; Kutas & Hillyard, 1984, 1989). First described by Kutas and Hillyard (1980), the N400 component has been extensively studied (see Kutas & Van Petten, 1988, 1994; Van Petten & Kutas, 1990 for a review). The classic N400 has a scalp distribution that is maximal over posterior scalp locations, particularly the parietal central (Pz) and centroparietal (CPz) electrodes. Furthermore, the N400 is thought to be sensitive to many of the same manipulations as semantic priming. Thus, in the current research we focused on the amplitude and latency of the N400 component as our ERP dependent measures of semantic processing in the cerebral hemispheres. As language stimuli we chose one of the more common linguistic tools that have been used to study hemispheric differences in semantic processing, the examination of word meaning retrieval for lexically ambiguous words (Atchley, Burgess, Audet, & Arambel, 1996; Atchley, Burgess, & Keeney, 1999a, 1999b; Burgess & Simpson, 1988; Chiarello, 1991; Faust & Chiarello, 1998; Koivisto, 1997; Nakagawa, 1991). In a lexical decision, priming experiment using ambiguous words as the primes (such as BANK) and one of its meanings as the targets (MONEY or RIVER), Burgess and Simpson (1988) were the first to show a time course dependent hemispheric processing dichotomy. When provided with a very short amount of time to process the prime word (35 ms), the left hemisphere (LH) shows priming for both dominant (MONEY) and subordinate (RIVER) meanings. The right hemisphere (RH) takes more time to activate both meanings (by at least 300 ms as established by Atchley et al., 1996; Chiarello, Maxfield, & Kahan, 1995; Koivisto, 1997). The more important difference between the two hemispheres, however, occurs after this initial activation phase of lexical retrieval. At a longer prime processing duration (750 ms), the LH shows no priming for the subordinate meaning of the word. In contrast, the RH shows sustained priming for both meanings of the ambiguous word (Burgess & Simpson, 1988). Burgess and Simpson hypothesized that this processing difference may be advantageous for the disambiguation of these ambiguous words during normal sentence processing. In normal circumstances, the LH makes a meaning selection and deactivates the contextually inappropriate meaning of the word. However, in sentences where the LH makes an error in its selection, the role of the RH may be to supply the alternative meaning. Because the most consistent differences between hemispheres are seen using a
long prime presentation duration, we used this duration for the current study. When making predictions for the current ERP study, a simple assumption would be that conditions in the DVF ambiguous word task that led to a response time advantage (i.e., related trials) would result in smaller N400s as compared to unrelated trials. A smaller N400 has been shown to occur when there is a high degree of semantic compatibility between the prime and target words as compared to trials where the target is preceded by an unrelated prime (Anderson & Holcomb, 1995; Holcomb & Neville, 1990; Rosler, Streb, & Haan, 2001). For this reason, we predicted that there would a large difference in the magnitude of the N400 between related and unrelated targets for both dominant (BANK– MONEY) and subordinate (BANK–RIVER) trials if the targets were presented to the RH. Additionally, we predicted that targets related to the dominant meaning of the ambiguous word, when presented to the LH, would also lead to a smaller magnitude N400 for related as compared to unrelated trials. In contrast, we predicted that subordinate related and unrelated targets should both lead to a large magnitude N400 and so there should be little difference between the related and unrelated waveforms for subordinate targets presented to the LH. This pattern of predictions is reasonable given earlier findings in the DVF literature, however, it is important to note that this assumes that priming magnitude and N400 magnitude are going to behave exactly the same way. Again, given the fact the ERPs seem to reflect semantic access at one point in the language comprehension time course, it is possible that N400 and priming magnitudes will be dissimilar because they reflect mechanisms occurring at different points in the processing stream.
2. Methods 2.1. Participants Eight students (seven females) from the University of Kansas undergraduate population participated in order to receive course credit in their introductory psychology course. Participants were all native English speakers, right handed, and reported no history of developmental language problems or neurological disorders. 2.2. Stimuli and procedure Stimuli were adopted from previous research done by the first author (Atchley et al., 1996; Atchley et al., 1999a, 1999b). There were a total of 160 experimental trials presented to each participant. The research design consisted of three within-participant independent variables: word meaning dominance (dominant vs. subor-
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dinate), prime-target relatedness (related vs. unrelated), and visual field of target presentation (left visual field (LVF) vs. right visual field (RVF)). There were an equal number of randomly presented trials in each of these eight conditions. Words were presented in white lettering on a black background. Dominant and subordinate targets were balanced for both word length and production frequency. Ambiguous prime words were presented centrally while targets were presented in a lateralized position that began 2° from central fixation and subtended a maximum of 5° of visual angle. Throughout the experiment participants sat in a comfortable, padded chair in a copper shielded suit of rooms. Participants were first exposed to 35 practice trials in order to help them become familiar with the lateralized presentation procedure. Each trial started with a central fixation cross that was presented for 500 ms. The prime was presented next for 750 ms. Targets were presented for 165 ms and were masked. Participants were told that they should push the 1 key on a response pad if the prime-target pairs were semantically related and the 2 key if the pair was unrelated. The stimuli were organized into two blocks of experimental trials. Each block took about 7.5 min to complete.
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task and were actively engaged. Given that overall accuracy was 68% reaction time analysis will not be reported. However, we did examine reaction time data to ensure that there were no speed accuracy trade-offs, and none were observed. The research design included in the following response accuracy ANOVAs was a three factor, within-participant design containing the variables of meaning dominance, prime-target relatedness, and visual field of target presentation. For the behavioral data, all three independent variables resulted in a main effect. Dominant targets (71%) were responded to more accurately than subordinate targets (61%, F ð1; 7Þ ¼ 9:33, p < :05). Targets presented to the LVF (60%) were responded to less accurately than targets presented to the RVF (73%, F ð1; 7Þ ¼ 14:87, p < :01). And finally, related word pairs were more accurate (78%) than unrelated word pairs (55%, F ð1; 7Þ ¼ 46:53, p < :001). Only the interaction between visual field and relatedness (F ð1; 7Þ ¼ 5:54, p < :05) was significant for the behavioral data. This interaction indicates that there was a greater advantage of primetarget relatedness if the targets were presented to the LVF (related: 75%, unrelated: 44%) than when the targets are presented to the RVF (related 81%, unrelated: 65%).
2.3. Electrophysiological recording 3.2. N400 analyses The electroencephalogram (EEG) was recorded with silver–silver chloride electrodes mounted in a commercially available ‘‘Quick cap.’’ Midline frontal (Fz), middle temporal (Tz), centroparietal (CPz), and parietal (Pz) recording sites were used, as defined by the 10–20 system. Each scalp site was referred to the linked mastoids. All electrode impedance was lower than 5K. Electrodes were placed above and below the left eye and at the outer canthi to monitor blinks and eye movements. The EEG was amplified with a NeuroScan Synamps amplifier with bandpass cutoffs of 0.01 and 50 Hz, digitized on-line with a sampling rate of 250 Hz. NeuroscanÕs eye movement correction protocol was used for eye movement correction. Trials with movement artifacts of greater than 70 mV were rejected during analysis. ERPs were timelocked to the onset of lateralized target word. Each averaged waveform for each experimental condition is calculated based on 20 trials per participant. The data were recorded and stored on a Pentium II 400 MHz, with an 18 GB hard disk.
3. Results 3.1. Behavioral semantic relatedness judgment data It is necessary to consider the behavioral data generated during the semantic relatedness judgement task so that we can establish that participants understood the
As in other paradigms using visual words the ERPs were characterized by a number of early components including the N1–P2 complex and an N2 component. In order to run an ANOVA on the obtained data, mean voltages across six, 50 ms time windows were considered 350–400, 400–450, 450–500, 500–550, 550–600, and 600– 650. The initial ANOVAs also included the variables of word meaning dominance, visual field of target, primetarget relatedness, and scalp site (four levels: Pz, CPz, Tz, and Fz) as factors. These analyses yielded only a main effect of channel (F ð3; 21Þ ¼ 28:37, p < :0001). A three-way interaction between meaning, visual field, and relatedness was significant (F ð1; 7Þ ¼ 12:21, p < :05) as was an interaction between visual field, channel, and time point (F ð15; 105Þ ¼ 4:07, p < :01). Planned comparisons were run to test the predictions summarized at the end of the introduction. First, an analysis was done for each individual electrode site to determine if there was a difference between the related and unrelated trials for either the dominant or subordinate targets. For the CPz electrode there was a significant interaction between meaning, visual field, and relatedness for the time period from 400–600 ms (F ð1; 7Þ ¼ 15:96, p < :01). t Tests were run for each of the 5 ms segments that make up this critical period in order to allow for peak-to-peak comparisons of the N400 amplitude generated by related and unrelated trials. t Tests indicated that the three-way interaction
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seen using an ANOVA was due to a significant difference in the N400 pattern between the two hemispheres. For a clearer understanding of these results obtained for the CPz electrode please see Fig. 1. In the RVF/LH trials there was a significant negative going wave for the unrelated trials that peaked at around 440 ms for the dominant trials (T ð7Þ ¼ 3:11, p < :01). This significant difference (of about 5 lV) in N400 amplitude for unrelated as compared to related trials is consistent with our a priori predictions. In addition to the N400 seen for dominant targets, there was also a significant negative going wave (or about 4 lV) for only the unrelated subordinate trials (T ð7Þ ¼ 2:15, p < :05) that peaked at around 560 ms, a latency delay of about 120 ms as compared to dominant trials. The presence of a significant N400 component for subordinate trials in the RVF/LH was inconsistent with our predictions. We predicted that there would be no difference between the subordinate related and unrelated trials in N400 amplitude. For both dominant and subordinate trials presented to the LVF/RH there was no difference between the related and unrelated trials (T ’s < 1). This null effect appears to be due to a complete lack of a negative going
wave for all targets presented to the LVF/RH. Again, this finding is inconsistent with our a priori predictions. We expected a significant difference in N400 amplitude for related and unrelated trials in both the dominant and subordinate conditions in the LVF/RH. There were no significant three-way interactions for any of the other channels examined, though the interaction of meaning, visual field, and relatedness did approach significance for the Pz electrode site (F ð1; 7Þ ¼ 3:98, p ¼ :08).
4. Discussion As was found by Federmeier and Kutas (1999), the magnitude of the N400 ERP component does seem to be sensitive to hemispheric differences in semantic processing. The pattern of the ERP waveforms for the two hemispheres are significantly different over posterior sites when you consider the time period from 400– 600 ms after the initial presentation of the lateralized target word. However, regarding the specific pattern of N400s predicted for waveforms elicited by dominant and subordinate targets in the two hemispheres, the predictions made based on the behavioral DVF litera-
Fig. 1. Interaction of meaning dominance, visual field, and relatedness for CPz electrode.
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ture were not confirmed. There were two aspects of the current data that were in direct contradiction to our expectations. First, we expect to see a significant difference between related and unrelated trials for both meaning conditions when targets were presented to the LVF/RH. Secondly, we did not expect to see a significant difference in the N400 amplitude when we compared subordinate related (BANK–RIVER) to unrelated trials presented to the RVF/LH and yet we did find a difference in N400 amplitude for these two trial types. Our predictions for the LVF/RH results were based both on conclusions drawn from DVF priming results and also based on results from Federmeier and Kutas (1999) who demonstrated that LVF word presentation leads to a equally large N400 for multiple kinds of semantically incompatible sentence final words. Contrary to our predictions, targets presented to the LVF/RH resulted in the complete lack of an N400 for both related and unrelated trials. At first glance this result may seem inconsistent with what has been found previously. However, let us consider that multiple researchers have argued that the RH is able to sustain access to a very broad or coarse representation of a wordÕs meaning (Atchley et al., 1999a, 1999b; Beeman, 1993; Beeman et al., 1994; Chiarello, 1991; Chiarello, Burgess, Richards, & Pollock, 1990; Faust, 1999). Therefore, one might actually expect that all LVF/RH targets that are preceded by a single, ambiguous prime word would result in small amplitude N400 because none of the targets are sufficiently semantically unexpected, not even unrelated targets. In other words, it might be the case that the RH, when faced with an impoverished semantic context, generates no semantic expectations and, as a result, shows no N400. This N400 pattern, if replicated, would suggest that the N400 ERP component and traditional behavioral priming results might diverge in very interesting ways which might reflect processing at multiple stages in the language comprehension time course. Likewise, the results obtained for subordinate targets presented to the RVF/LH also diverge in an intriguing way from the general findings using behavioral measures. We expected that subordinate related trials in the RVF/ LH would lead to an N400 amplitude that was as large as the N400 generated by unrelated trials. This predicted pattern would have been consistent with the idea that the LH uses a selective mechanism to limit word meaning access to only the most dominant meaning of a lexically ambiguous word. Instead we found a significantly smaller N400 amplitude for the related subordinate trials as compared to the unrelated trials. Additionally, we found that the latency of this peak-to-peak difference between related and unrelated trials was about 120 ms after the negative wave shown for dominant targets. Thus, we do see evidence for an N400 in subordinate trials for the RVF/LH but this N400 is delayed as com-
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pared to the dominant meaning condition. As with the LVF/RH results, our interpretation of this finding needs to be cautious given the singularity of these results. However, these results should be taken to indicate that both N400 amplitude and latency might be important measures to consider in DVF research, particularly given that for the RVF/LH latency mirrors the previous behavioral priming results more closely than does the amplitude dependent measure. The current research represents an important step in the coalescence of two mature research methodologies, DVF and electrophysiology. Results indicate that ERPs, in particular the latency and amplitude of the N400 ERP component, are sensitive to hemispheric differences in semantic processing. Furthermore, we found that the pattern of N400 amplitudes and latencies did not simply mimic behavioral response data. Instead, using ERP components as a dependent measure of hemispheric semantic processing may provide new information about the function of each cerebral hemisphere.
Acknowledgments This research was supported by the National Science Foundation under Grant No. 0078778 awarded to the first author.
References Anderson, J., & Holcomb, P. (1995). Auditory and visual semantic priming using different stimulus onset asynchronies: An eventrelated brain potential study. Psychophysiology, 32, 177–190. Atchley, R. A., Burgess, C., Audet, C., & Arambel, S. (1996). Timecourse, context effects, and the processing of lexical ambiguity in the cerebral hemispheres. Brain and Cognition, 30, 257–261. Atchley, R. A., Burgess, C., & Keeney, M. (1999a). The effects of timecourse and context on the facilitation of semantic features in the cerebral hemispheres. Neuropsychology, 13, 389–403. Atchley, R. A., Keeney, M., & Burgess, C. (1999b). Cerebral hemispheric mechanisms linking ambiguous word meaning retrieval and creativity. Brain and Cognition, 30, 479–499. Beeman, M. (1993). Semantic processing in the right hemisphere may contribute to drawing inferences from discourse. Brain and Language, 44, 80–120. Beeman, M., & Chiarello, C. (1998). Right hemisphere language comprehension: Perspectives from cognitive neuroscience. Hillsdale, NJ: Lawrence Erlbaum Associates. Beeman, M., Friedman, R., Grafman, J., Perez, E., Diamond, S., & Lindsay, M. (1994). Summation priming and coarse semantic coding in the right hemisphere. Journal of Cognitive Neuroscience, 6, 26–43. Burgess, C., & Simpson, G. (1988). Cerebral hemispheric mechanisms in the retrieval of ambiguous word meanings. Brain and Language, 33, 86–103. Chiarello, C. (1991). Interpretation of word meanings by the cerebral hemispheres: One is not enough. In P. Schwanenflugel (Ed.), The psychology of word meanings. Hillsdale, NJ: Erlbaum. Chiarello, C., Burgess, C., Richards, L., & Pollock, A. (1990). Semantic and associative priming in the cerebral hemispheres:
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Some words do, some words donÕt sometimes, some places. Brain and Language, 38, 75–104. Chiarello, C., Maxfield, L., & Kahan, T. (1995). Initial right hemisphere activation of subordinate word meanings is not due to homotopic callosal inhibition. Psychonomic Bulletin & Review, 2, 375–380. Faust, M. (1999). Obtaining evidence of language comprehension from sentence priming. In M. Beeman, & C. Chiarello (Eds.), Right hemisphere language comprehension: Perspectives from cognitive neuroscience. Hillsdale, NJ: Erlbaum. Faust, M., & Chiarello, C. (1998). Sentence context and lexical ambiguity resolution by the two hemispheres. Neuropsychologia, 36, 827–835. Federmeier, K., & Kutas, M. (1999). Right words and left words: Electrophysiological evidence for hemispheric differences in meaning processing. Cognitive Brain Research, 8, 373–392. Holcomb, P., & Neville, H. (1990). Auditory and visual semantic priming in lexical decision: A comparison using event-related potentials. Language and Cognitive Processes, 5, 281–312. Koivisto, M. (1997). Time course of semantic activation in the cerebral hemispheres. Neuropsychologia, 35, 497–504. Kutas, M. (1993). In the company of other words: Electrophysiological evidence for single-word and sentence context effects. Language and Cognitive Process, 8, 533–572. Kutas, M., & Hillyard, S. A. (1980). Reading senseless sentences: Brain potentials reflect semantic incongruity. Science, 207, 203–205. Kutas, M., & Hillyard, S. A. (1984). Brain potentials during reading reflect word expectancy and semantic association. Nature, 307, 1161–1163.
Kutas, M., & Hillyard, S. A. (1989). An electrophysiological probe of incidental semantic associations. Journal of Cognitive Science, 1, 38–49. Kutas, M., & Van Petten, C. K. (1988). Event-related potential studies of language. In P. K. Ackles, J. R. Jennings, & M. G. H. Coles (Eds.), Advances in psychophysiology. Greenwich, CT: JAI Press. Kutas, M., & Van Petten, C. K. (1994). Psycholinguistics electrified. In M. A. Gernsbacher (Ed.), Handbook of psycholinguistics. New York: Academic Press. McCarthy, G., & Nobre, A. (1993). Modulation of semantic processing by spatial selective attention. Electroencephalography and Clinical Neurophysiology, 88, 210–219. McCarthy, G., & Wood, C. (1985). Scalp distributions of event-related potentials: An ambiguity associated with analysis of variance models. Electroencephalography and Clinical Neurophysiology, 62, 203–208. Nakagawa, A. (1991). Role of anterior and posterior attention networks in hemispheric asymmetries during lexical decisions. Journal of Cognitive Neuroscience, 3, 315–321. Rosler, F., Streb, J., & Haan, H. (2001). Event-related potentials evoked by verbs and nouns in a primed lexical decision task. Psychophysiology, 38, 694–703. Swaab, T., Baynes, K., & Knight, R. (1998). Course semantic coding in the right hemisphere: An ERP study. Journal of Cognitive Neuroscience Supplement, 1, 34. Van Petten, C., & Kutas, M. (1990). Interactions between sentence context and word frequency in event-related potentials. Memory & Cognition, 18, 380–393.
Using event-related potentials to examine hemispheric differences in semantic processing Ruth Ann Atchley and Kristin M. Kwasny University of Kansas, Lawrence, KS 66045, USA Accepted 7 May 2003
Abstract Event-related potentials (ERPs) were used as the dependent measure in a divided visual field study examining the processing of lexically ambiguous words in the cerebral hemispheres. The goal was to determine if the N400 ERP component is sensitive measure of hemispheric differences in semantic processing. ERP waveforms were examined for lateralized target words that were related to either the dominant (MONEY) or subordinate (RIVER) meanings of ambiguous words (BANK). These waveforms were compared to trials where the prime-target pairs were unrelated. Reliable N400s, reflecting a significant difference between related and unrelated trials, were seen when targets were presented to the right visual field/left hemisphere. However, there were no N400s observed for either the dominant or subordinate conditions when targets were presented to the left visual field/right hemisphere. Ó 2003 Elsevier Inc. All rights reserved.
1. Introduction Divided visual field (DVF) techniques have effectively been used as an method for examining hemispheric differences in lexical and semantic processing and have resulted in the development of a number of interesting models that postulate that both cerebral hemispheres contribute to language comprehension (see Beeman & Chiarello, 1998 for a review). The current study represents an important extension of this research in that both DVF stimulus presentation and event-related potentials (ERPs) are employed as dependent measures. Traditionally, behavioral dependent measures (such as naming or lexical decision) have been used in DVF studies and in particular the magnitude of priming (or the difference in reaction time or accuracy between related and unrelated trials) is commonly examined. Very little research has been done that uses ERPs to examine lateralized semantic processing (Federmeier & Kutas, 1999; McCarthy & Nobre, 1993; Swaab, Baynes, & Knight, 1998). The combination of DVF stimulus presentation and electrophysiological measurement will significantly contribute to the current literature because it provides information that cannot be gained with either behavioral measures alone or with electrophysiological 0278-2626/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved. doi:10.1016/S0278-2626(03)00095-2
measures using central visual field stimulus presentation. First, ERPs provide insight into the time course of language comprehension because they can provide data that reflect processing at each millisecond of the comprehension process (see Kutas & Van Petten, 1994). In contrast, behavioral measures reflect the summation of all the steps that elapse prior to the language taskÕs behavioral response. Regarding issues of cerebral lateralization, it is hard to draw conclusions regarding localization of function when considering ERP data because of the inverse problem inherent in most ERP research (McCarthy & Wood, 1985). We can avoid making potentially problematic assumptions based on conclusions drawn from the scalp distribution of the ERP waveforms by employing a DVF presentation of the targets. Lateralized presentation of stimuli leads to robust and reliable differences in word processing when response time and response accuracy are measured across a number of language tasks (Beeman & Chiarello, 1998). Therefore, it is reasonable to assume that this presentation technique should also influence ERP components in a way that should reflect hemispheric differences in language processing. One of the major goals of the current research was to determine if this assumption is well founded; to determine if ERP
134
R. Ann Atchley, K.M. Kwasny / Brain and Cognition 53 (2003) 133–138
components are sensitive to hemispheric difference in language processing. One ERP component, referred to as the N400, is particularly sensitive to the semantic aspects of experimental stimuli and the magnitude of this waveform seems to be a reflection of the semantic compatibility between sequentially presented words (Kutus & Van Petten, 1994; Kutas, 1993; Kutas & Hillyard, 1984, 1989). First described by Kutas and Hillyard (1980), the N400 component has been extensively studied (see Kutas & Van Petten, 1988, 1994; Van Petten & Kutas, 1990 for a review). The classic N400 has a scalp distribution that is maximal over posterior scalp locations, particularly the parietal central (Pz) and centroparietal (CPz) electrodes. Furthermore, the N400 is thought to be sensitive to many of the same manipulations as semantic priming. Thus, in the current research we focused on the amplitude and latency of the N400 component as our ERP dependent measures of semantic processing in the cerebral hemispheres. As language stimuli we chose one of the more common linguistic tools that have been used to study hemispheric differences in semantic processing, the examination of word meaning retrieval for lexically ambiguous words (Atchley, Burgess, Audet, & Arambel, 1996; Atchley, Burgess, & Keeney, 1999a, 1999b; Burgess & Simpson, 1988; Chiarello, 1991; Faust & Chiarello, 1998; Koivisto, 1997; Nakagawa, 1991). In a lexical decision, priming experiment using ambiguous words as the primes (such as BANK) and one of its meanings as the targets (MONEY or RIVER), Burgess and Simpson (1988) were the first to show a time course dependent hemispheric processing dichotomy. When provided with a very short amount of time to process the prime word (35 ms), the left hemisphere (LH) shows priming for both dominant (MONEY) and subordinate (RIVER) meanings. The right hemisphere (RH) takes more time to activate both meanings (by at least 300 ms as established by Atchley et al., 1996; Chiarello, Maxfield, & Kahan, 1995; Koivisto, 1997). The more important difference between the two hemispheres, however, occurs after this initial activation phase of lexical retrieval. At a longer prime processing duration (750 ms), the LH shows no priming for the subordinate meaning of the word. In contrast, the RH shows sustained priming for both meanings of the ambiguous word (Burgess & Simpson, 1988). Burgess and Simpson hypothesized that this processing difference may be advantageous for the disambiguation of these ambiguous words during normal sentence processing. In normal circumstances, the LH makes a meaning selection and deactivates the contextually inappropriate meaning of the word. However, in sentences where the LH makes an error in its selection, the role of the RH may be to supply the alternative meaning. Because the most consistent differences between hemispheres are seen using a
long prime presentation duration, we used this duration for the current study. When making predictions for the current ERP study, a simple assumption would be that conditions in the DVF ambiguous word task that led to a response time advantage (i.e., related trials) would result in smaller N400s as compared to unrelated trials. A smaller N400 has been shown to occur when there is a high degree of semantic compatibility between the prime and target words as compared to trials where the target is preceded by an unrelated prime (Anderson & Holcomb, 1995; Holcomb & Neville, 1990; Rosler, Streb, & Haan, 2001). For this reason, we predicted that there would a large difference in the magnitude of the N400 between related and unrelated targets for both dominant (BANK– MONEY) and subordinate (BANK–RIVER) trials if the targets were presented to the RH. Additionally, we predicted that targets related to the dominant meaning of the ambiguous word, when presented to the LH, would also lead to a smaller magnitude N400 for related as compared to unrelated trials. In contrast, we predicted that subordinate related and unrelated targets should both lead to a large magnitude N400 and so there should be little difference between the related and unrelated waveforms for subordinate targets presented to the LH. This pattern of predictions is reasonable given earlier findings in the DVF literature, however, it is important to note that this assumes that priming magnitude and N400 magnitude are going to behave exactly the same way. Again, given the fact the ERPs seem to reflect semantic access at one point in the language comprehension time course, it is possible that N400 and priming magnitudes will be dissimilar because they reflect mechanisms occurring at different points in the processing stream.
2. Methods 2.1. Participants Eight students (seven females) from the University of Kansas undergraduate population participated in order to receive course credit in their introductory psychology course. Participants were all native English speakers, right handed, and reported no history of developmental language problems or neurological disorders. 2.2. Stimuli and procedure Stimuli were adopted from previous research done by the first author (Atchley et al., 1996; Atchley et al., 1999a, 1999b). There were a total of 160 experimental trials presented to each participant. The research design consisted of three within-participant independent variables: word meaning dominance (dominant vs. subor-
R. Ann Atchley, K.M. Kwasny / Brain and Cognition 53 (2003) 133–138
dinate), prime-target relatedness (related vs. unrelated), and visual field of target presentation (left visual field (LVF) vs. right visual field (RVF)). There were an equal number of randomly presented trials in each of these eight conditions. Words were presented in white lettering on a black background. Dominant and subordinate targets were balanced for both word length and production frequency. Ambiguous prime words were presented centrally while targets were presented in a lateralized position that began 2° from central fixation and subtended a maximum of 5° of visual angle. Throughout the experiment participants sat in a comfortable, padded chair in a copper shielded suit of rooms. Participants were first exposed to 35 practice trials in order to help them become familiar with the lateralized presentation procedure. Each trial started with a central fixation cross that was presented for 500 ms. The prime was presented next for 750 ms. Targets were presented for 165 ms and were masked. Participants were told that they should push the 1 key on a response pad if the prime-target pairs were semantically related and the 2 key if the pair was unrelated. The stimuli were organized into two blocks of experimental trials. Each block took about 7.5 min to complete.
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task and were actively engaged. Given that overall accuracy was 68% reaction time analysis will not be reported. However, we did examine reaction time data to ensure that there were no speed accuracy trade-offs, and none were observed. The research design included in the following response accuracy ANOVAs was a three factor, within-participant design containing the variables of meaning dominance, prime-target relatedness, and visual field of target presentation. For the behavioral data, all three independent variables resulted in a main effect. Dominant targets (71%) were responded to more accurately than subordinate targets (61%, F ð1; 7Þ ¼ 9:33, p < :05). Targets presented to the LVF (60%) were responded to less accurately than targets presented to the RVF (73%, F ð1; 7Þ ¼ 14:87, p < :01). And finally, related word pairs were more accurate (78%) than unrelated word pairs (55%, F ð1; 7Þ ¼ 46:53, p < :001). Only the interaction between visual field and relatedness (F ð1; 7Þ ¼ 5:54, p < :05) was significant for the behavioral data. This interaction indicates that there was a greater advantage of primetarget relatedness if the targets were presented to the LVF (related: 75%, unrelated: 44%) than when the targets are presented to the RVF (related 81%, unrelated: 65%).
2.3. Electrophysiological recording 3.2. N400 analyses The electroencephalogram (EEG) was recorded with silver–silver chloride electrodes mounted in a commercially available ‘‘Quick cap.’’ Midline frontal (Fz), middle temporal (Tz), centroparietal (CPz), and parietal (Pz) recording sites were used, as defined by the 10–20 system. Each scalp site was referred to the linked mastoids. All electrode impedance was lower than 5K. Electrodes were placed above and below the left eye and at the outer canthi to monitor blinks and eye movements. The EEG was amplified with a NeuroScan Synamps amplifier with bandpass cutoffs of 0.01 and 50 Hz, digitized on-line with a sampling rate of 250 Hz. NeuroscanÕs eye movement correction protocol was used for eye movement correction. Trials with movement artifacts of greater than 70 mV were rejected during analysis. ERPs were timelocked to the onset of lateralized target word. Each averaged waveform for each experimental condition is calculated based on 20 trials per participant. The data were recorded and stored on a Pentium II 400 MHz, with an 18 GB hard disk.
3. Results 3.1. Behavioral semantic relatedness judgment data It is necessary to consider the behavioral data generated during the semantic relatedness judgement task so that we can establish that participants understood the
As in other paradigms using visual words the ERPs were characterized by a number of early components including the N1–P2 complex and an N2 component. In order to run an ANOVA on the obtained data, mean voltages across six, 50 ms time windows were considered 350–400, 400–450, 450–500, 500–550, 550–600, and 600– 650. The initial ANOVAs also included the variables of word meaning dominance, visual field of target, primetarget relatedness, and scalp site (four levels: Pz, CPz, Tz, and Fz) as factors. These analyses yielded only a main effect of channel (F ð3; 21Þ ¼ 28:37, p < :0001). A three-way interaction between meaning, visual field, and relatedness was significant (F ð1; 7Þ ¼ 12:21, p < :05) as was an interaction between visual field, channel, and time point (F ð15; 105Þ ¼ 4:07, p < :01). Planned comparisons were run to test the predictions summarized at the end of the introduction. First, an analysis was done for each individual electrode site to determine if there was a difference between the related and unrelated trials for either the dominant or subordinate targets. For the CPz electrode there was a significant interaction between meaning, visual field, and relatedness for the time period from 400–600 ms (F ð1; 7Þ ¼ 15:96, p < :01). t Tests were run for each of the 5 ms segments that make up this critical period in order to allow for peak-to-peak comparisons of the N400 amplitude generated by related and unrelated trials. t Tests indicated that the three-way interaction
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seen using an ANOVA was due to a significant difference in the N400 pattern between the two hemispheres. For a clearer understanding of these results obtained for the CPz electrode please see Fig. 1. In the RVF/LH trials there was a significant negative going wave for the unrelated trials that peaked at around 440 ms for the dominant trials (T ð7Þ ¼ 3:11, p < :01). This significant difference (of about 5 lV) in N400 amplitude for unrelated as compared to related trials is consistent with our a priori predictions. In addition to the N400 seen for dominant targets, there was also a significant negative going wave (or about 4 lV) for only the unrelated subordinate trials (T ð7Þ ¼ 2:15, p < :05) that peaked at around 560 ms, a latency delay of about 120 ms as compared to dominant trials. The presence of a significant N400 component for subordinate trials in the RVF/LH was inconsistent with our predictions. We predicted that there would be no difference between the subordinate related and unrelated trials in N400 amplitude. For both dominant and subordinate trials presented to the LVF/RH there was no difference between the related and unrelated trials (T ’s < 1). This null effect appears to be due to a complete lack of a negative going
wave for all targets presented to the LVF/RH. Again, this finding is inconsistent with our a priori predictions. We expected a significant difference in N400 amplitude for related and unrelated trials in both the dominant and subordinate conditions in the LVF/RH. There were no significant three-way interactions for any of the other channels examined, though the interaction of meaning, visual field, and relatedness did approach significance for the Pz electrode site (F ð1; 7Þ ¼ 3:98, p ¼ :08).
4. Discussion As was found by Federmeier and Kutas (1999), the magnitude of the N400 ERP component does seem to be sensitive to hemispheric differences in semantic processing. The pattern of the ERP waveforms for the two hemispheres are significantly different over posterior sites when you consider the time period from 400– 600 ms after the initial presentation of the lateralized target word. However, regarding the specific pattern of N400s predicted for waveforms elicited by dominant and subordinate targets in the two hemispheres, the predictions made based on the behavioral DVF litera-
Fig. 1. Interaction of meaning dominance, visual field, and relatedness for CPz electrode.
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ture were not confirmed. There were two aspects of the current data that were in direct contradiction to our expectations. First, we expect to see a significant difference between related and unrelated trials for both meaning conditions when targets were presented to the LVF/RH. Secondly, we did not expect to see a significant difference in the N400 amplitude when we compared subordinate related (BANK–RIVER) to unrelated trials presented to the RVF/LH and yet we did find a difference in N400 amplitude for these two trial types. Our predictions for the LVF/RH results were based both on conclusions drawn from DVF priming results and also based on results from Federmeier and Kutas (1999) who demonstrated that LVF word presentation leads to a equally large N400 for multiple kinds of semantically incompatible sentence final words. Contrary to our predictions, targets presented to the LVF/RH resulted in the complete lack of an N400 for both related and unrelated trials. At first glance this result may seem inconsistent with what has been found previously. However, let us consider that multiple researchers have argued that the RH is able to sustain access to a very broad or coarse representation of a wordÕs meaning (Atchley et al., 1999a, 1999b; Beeman, 1993; Beeman et al., 1994; Chiarello, 1991; Chiarello, Burgess, Richards, & Pollock, 1990; Faust, 1999). Therefore, one might actually expect that all LVF/RH targets that are preceded by a single, ambiguous prime word would result in small amplitude N400 because none of the targets are sufficiently semantically unexpected, not even unrelated targets. In other words, it might be the case that the RH, when faced with an impoverished semantic context, generates no semantic expectations and, as a result, shows no N400. This N400 pattern, if replicated, would suggest that the N400 ERP component and traditional behavioral priming results might diverge in very interesting ways which might reflect processing at multiple stages in the language comprehension time course. Likewise, the results obtained for subordinate targets presented to the RVF/LH also diverge in an intriguing way from the general findings using behavioral measures. We expected that subordinate related trials in the RVF/ LH would lead to an N400 amplitude that was as large as the N400 generated by unrelated trials. This predicted pattern would have been consistent with the idea that the LH uses a selective mechanism to limit word meaning access to only the most dominant meaning of a lexically ambiguous word. Instead we found a significantly smaller N400 amplitude for the related subordinate trials as compared to the unrelated trials. Additionally, we found that the latency of this peak-to-peak difference between related and unrelated trials was about 120 ms after the negative wave shown for dominant targets. Thus, we do see evidence for an N400 in subordinate trials for the RVF/LH but this N400 is delayed as com-
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pared to the dominant meaning condition. As with the LVF/RH results, our interpretation of this finding needs to be cautious given the singularity of these results. However, these results should be taken to indicate that both N400 amplitude and latency might be important measures to consider in DVF research, particularly given that for the RVF/LH latency mirrors the previous behavioral priming results more closely than does the amplitude dependent measure. The current research represents an important step in the coalescence of two mature research methodologies, DVF and electrophysiology. Results indicate that ERPs, in particular the latency and amplitude of the N400 ERP component, are sensitive to hemispheric differences in semantic processing. Furthermore, we found that the pattern of N400 amplitudes and latencies did not simply mimic behavioral response data. Instead, using ERP components as a dependent measure of hemispheric semantic processing may provide new information about the function of each cerebral hemisphere.
Acknowledgments This research was supported by the National Science Foundation under Grant No. 0078778 awarded to the first author.
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