ERP correlates of the bilateral redundancy gain for words

Neuropsychologia 45 (2007) 2114–2124

ERP correlates of the bilateral redundancy gain for words Bettina Mohr a,b,∗ , Tanja Endrass c , Olaf Hauk a , Friedemann Pulverm¨uller a a

Medical Research Council, Cognition and Brain Sciences Unit, Cambridge, UK b Department of Psychology, Anglia Ruskin University, Cambridge, UK c Institute of Psychology, Humboldt University Berlin, Berlin, Germany

Received 6 December 2005; received in revised form 16 January 2007; accepted 21 January 2007 Available online 30 January 2007

Abstract Neurophysiological correlates of hemispheric asymmetry and interhemispheric interaction in lexical processing were investigated in a lexical decision task with tachistoscopic stimulus presentation either unilaterally, to the right or left visual field, or bilaterally, with identical stimulus copies to each visual hemi-field. Behavioral data confirmed both right visual field advantage and bilateral redundancy gain for words but not for pronounceable orthographically regular pseudowords. ERPs showed a significant amplitude increase 160–200 after stimulus presentation specifically for words after bilateral redundant stimulation, which was present in the recordings from both hemispheres. Localization of cortical sources using minimum norm estimation indicated stronger cortical activity for words in temporal regions of both hemispheres after bilateral presentation compared with each of the unilateral stimulation conditions individually. Pseudoword presentation did not lead to a general increase of cortical activation in the bilateral condition compared with unilateral presentation. The specific activation increase for words in the bilateral redundant condition relative to unilateral stimulation and the absence of this effect for pseudowords, which became manifest in a significant interaction of the factors lexicality and presentation mode, is best explained by summation of neuronal activation from both hemispheres within distributed lexical circuits. Source estimation indicates that temporal areas, particularly in the left hemisphere, are the primary cortical loci where such stimulus-specific activity increases occurred. © 2007 Elsevier Ltd. All rights reserved. Keywords: Bilateral redundancy gain; Interhemispheric transfer; Lexical decision; Hemispheric asymmetry; ERP

1. Introduction In recent years, research on hemispheric function has moved on from hemispheric specialization to questions about the interaction of both cerebral hemispheres in specific cognitive processing. A main reason for this was the insight that most tasks, even strongly lateralized ones, as for example word recognition, can be carried out, at least to some degree, by both hemispheres (e.g., Zaidel, 1976). The question therefore arises how the two hemispheres join their forces in normal function. A range of methods is used to scrutinize hemispheric interaction in normal healthy individuals. One of the classic paradigms, the bilateral redundancy paradigm, involves the presentation of stimuli tachistoscopically unilaterally to either

the left (LVF) or right (RVF) visual hemi-field or simultaneously to both visual fields (BVF) (Beaumont & Dimond, 1973; Miller, 1982). Most frequently, the results obtained with the bilateral redundancy paradigm demonstrate a bilateral or bihemispheric processing advantage, also called bilateral advantage or bilateral redundancy gain (BRG), with significantly better behavioral performance in the bilateral condition compared to the best unilateral condition.1 The bilateral advantage has been reported for a range of stimuli. It occurs for elementary visual stimuli (Beaumont & Dimond, 1973; Miller, 1982), for example checkerboard patterns (Miniussi, Girelli, & Marzi, 1998), colours (Roser & Corballis, 2003), but its emergence for complex stimuli, such as letter strings

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∗

Corresponding author at: MRC-Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 7EF, UK. Tel.: +44 355294x733; fax: +44 359062. E-mail address: [email protected] (B. Mohr). 0028-3932/$ – see front matter © 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2007.01.015

The left hemisphere is dominant for language processing, and written words presented in the right visual field are therefore usually processed better than those shown on the left. In this case, the critical question is therefore whether performance in the bilateral presentation condition is superior to the right visual field condition, which is the better of the unilateral conditions.

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and faces, seems to depend on the nature of these items. Common consonant-vowel-consonant (cvc) syllables (Hellige, Taylor, & Eng, 1989; Marks & Hellige, 1999, 2003), words (Hasbrooke & Chiarello, 1998; Mohr, Pulverm¨uller, & Zaidel, 1994; Mohr, Pulverm¨uller, Mittelst¨adt, & Rayman, 1996; Mohr, Landgrebe, & Schweinberger, 2002), and familiar faces (Mohr et al., 2002; Schweinberger, Landgrebe, Mohr, & Kaufmann, 2003) apparently induce a bilateral gain. However, this effect is absent or greatly reduced for unfamiliar complex stimuli such as pseudowords (Mohr, Pulverm¨uller, & Zaidel, 1994, 1996) or unfamiliar faces (Mohr et al., 2002). Interestingly, the bilateral advantage for highly complex and familiar stimuli requires exact simultaneity of stimulus presentation (Mohr & Pulverm¨uller, 2002). Superior behavioral performance for bilateral over unilateral stimulation has consistently been reported after simultaneous stimulation with identical stimuli, but rather inconsistently when two or more different stimuli were presented at the same time. The latter paradigm may lead to a bilateral advantage when participants are dealing with complex tasks, whereas when solving a simple task, the advantage can be absent (Banich & Karol, 1992; Hellige et al., 1989). At the functional level, bilateral advantages speak against inhibitory mechanisms between the hemispheres but rather suggest interhemispheric facilitation in cognitive processing. Bilateral redundancy gains for elementary stimuli have been interpreted in the context of race models, according to which each hemisphere acts as an independent processor and the faster hemisphere in a given trial would determine the behavioral response (Miller, 1982). This model suggests an explanation of the bilateral gain in terms of added probabilities, which, however, was not always successful, as several studies reported super-additivity of the bilateral advantage for elementary stimuli (Beaumont & Dimond, 1973; Miniussi et al., 1998). However, other work using simple, meaningless stimuli such as false fonts (Murray, Foxe, Higgins, Javitt, & Schroeder, 2001) or light flashes (Corballis, 1998; Iacoboni & Zaidel, 2003; ReuterLorenz, Nozawa, Gazzaniga, & Hughes, 1995) did not confirm super-additivity of the bilateral gain to elementary stimuli in healthy individuals. The issue of super-additivity of the bilateral gain is therefore still under discussion. The stimulus-specificity of the bilateral advantage for complex stimuli eliciting higher cognitive processes, such as object, face or word recognition, constitutes a major challenge to a race model; therefore, alternative models have been sought (for discussion, see Mohr & Pulverm¨uller, 2002; Mohr, Pulverm¨uller, & Zaidel, 1994). The robust finding of a bilateral advantage for familiar and meaningful material and its absence, or great reduction, for matched unfamiliar stimuli has been related to the existence or absence of memory circuits in the human brain for a given stimulus (Mohr, Pulverm¨uller, & Zaidel, 1994; Mohr & Pulverm¨uller, 2002; Pulverm¨uller, 1999). A neurocognitive model rooted in Hebb’s cell assembly theory (Hebb, 1949) posits that, due to simultaneous co-activation of neurons in both hemispheres during production and understanding of words, or during the perception of faces and objects, strongly connected neuronal circuits are being formed. In this framework, memory circuits comprising neurons in both cerebral hemispheres (transcortical

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cell assemblies) with gradual laterality were therefore posited for familiar words and faces, but not for unfamiliar ones (Mohr et al., 2002; Pulverm¨uller & Mohr, 1996). Bilateral presentation of previously learned meaningful stimuli – but not unfamiliar ones – would thus activate neuronal assemblies distributed over both hemispheres, yielding fast interhemispheric summation of neuronal activity and, hence, speeded ignition of the entire assembly. At the behavioral level, these summation processes eventually lead to faster perception of a stimulus and, as neuronal summation would also lead to a greater and more reliable signal, more accurate performance. This explanation of the bilateral redundancy gain for familiar items by summation mechanisms in transcortical cell assemblies also accounts for its absence for unfamiliar stimuli, which are not assumed to be represented by transcortical cell assemblies. It also offers an account for the absence of the bilateral advantage for words in an acallosal patient (Mohr, Pulverm¨uller, Rayman, & Zaidel, 1994). However, results for patients without direct connection between the hemispheres are more variable, as some of these patients have been reported to show super-additive bilateral redundancy effects, especially for elementary stimuli. These super-additive effects were found for several patients with either callosotomy or callosal agenesis and were interpreted in terms of subcortical summation processes for elementary stimuli. The relevant summation processes have been attributed to the level of elementary visual processes in the superior colliculi (Corballis, 1998; Savazzi & Marzi, 2004) and to subcortical convergence of response-related activation (Roser & Corballis, 2003). The absence of ipsilateral early ERPs (including P1 and N1) in split-brain and acallosal patients demonstrates that the corpus callosum is necessary for interhemispheric activation transfer between cortical areas (Brown, Larson, & Jeeves, 1994; Brown & Jeeves, 1999).To investigate the neurobiological mechanisms underlying the bilateral processing advantage at the behavioral level, it is necessary to investigate this effect with brain imaging techniques. In an ERP study, Miniussi et al. (1998) looked at the neurophysiological mechanisms of the bilateral redundancy gain, or redundant target effect (RTE), obtained previously in behavioral studies. In a simple stimulus detection task where no complete identification of the stimuli were required, reactions to checkerboard patterns elicited shorter ERP latencies (C1, P1 and N1) in the bilateral condition relative to unilateral conditions. These data suggest that neuronal co-activation mechanisms over both hemispheres might already start at a rather early perceptual processing level, at least in the visual domain. The authors argue that the timing of the RTE is likely to depend on the paradigms applied and on the cognitive processing stage required by the task (Miniussi et al., 1998). In line with this, Iacoboni and Zaidel (2003) attribute the bilateral advantage to one or more cognitive – and possibly brain loci – motor, perceptual and cognitive, and report a change in brain metabolism with bilateral targets in premotor cortex. A differential neurophysiological effect to familiar and unfamiliar stimuli inducing higher cognitive processes has been reported by Endrass, Mohr, & Pulverm¨uller (2004). Following Pulverm¨uller et al. (2001), Pulverm¨uller and Shtyrov (2003), Shtyrov and Pulverm¨uller (2002), these authors investigated

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spoken word and pseudoword processing using a mismatch negativity (MMN) design. Results showed a larger mismatch negativity brain response to binaurally presented words than to pseudowords, which they attributed to the amplifying effect of the strongly connected memory circuits for spoken words (Pulverm¨uller et al., 2001). Endrass et al. (2004) presented words monaurally or binaurally and found a significant increase of activation for binaural word presentation, but relatively weak activation for pseudowords across presentation conditions. This result is consistent with the behavioral findings in the visual modality (Mohr, Pulverm¨uller, Cohen, & Rockstroh, 2000; Mohr et al., 1996; Mohr, Pulverm¨uller, & Zaidel, 1994) and is best explained by neuronal summation at the cognitive level, possibly mediated by transcortical cell assemblies processing words. However, as Endrass’ study still leaves open the possibility that interactions between contralateral and ipsilateral auditory pathways led to redundancy effects, rather than the connections through the callosum, it appears imperative to study the physiology of the cognitive bilateral advantage in a fully crossed system, that is in the visual domain. When can the neurophysiological correlates of the bilateral advantage at the cognitive level be expected to emerge? Previous studies have demonstrated early (ranging from 100–150 ms to 150–200 ms after stimulus onset) differential activation between words and pseudowords and words from various word categories. Pulverm¨uller, Lutzenberger, and Birbaumer (1995) showed hemispheric differences between function and content words at 150–180 ms after stimulus presentation onset. Other studies observed similarly early ERP differences as a function of semantic content (Pulverm¨uller, Lutzenberger, & Preissl, 1999; Skrandies, 1998), syntactic properties (Shtyrov & Pulverm¨uller, 2002) and emotional valence of words (Begleiter & Platz, 1969; Bernat, Bunce, & Shevrin, 2001; Ortigue et al., 2004). Similarly, early ERP differences between words and matched pseudowords were reported in the visual and acoustic domain (150–200 ms; Endrass et al., 2004; see also Pulverm¨uller, 1999, 2005 for a review). Recent research indicated that the ultra-early effects (at ∼100 ms; e.g., Compton, Grossenbacher, Posner, & Tucker, 1991) may not be due to the word/pseudoword distinction itself but rather to a frequent confound of this distinction, namely differences in letter bigram frequencies (Hauk, Davis, Ford, Pulverm¨uller, & Marslen-Wilson, 2006; Hauk, Patterson, et al., 2006). Therefore, we expected to find electrocortical correlates of the bilateral redundancy gain for words between 150 and 200 ms after stimulus onset. The present study was designed to investigate the neurophysiological mechanisms underlying interhemispheric cooperation in the visual domain when meaningful words are being processed. The aim was to find an electrocortical correlate of the cognitive differential bilateral advantage demonstrated in previous behavioral studies. In a lexical decision task, words and pseudowords were presented either to the LVF or to the RVF, or bilaterally with two identical copies of a stimulus simultaneously flashed to both visual hemi-fields (BVF). Electrophysiological activity was recorded with a 64 channel EEG system to allow for both monitoring of exact temporal dynamics and estimation of critical cortical sources.

We expected the behavioral data to show a replication of a right visual field advantage (RVFA) and the bilateral advantage for words, but absence of these effects for pseudowords. A neurophysiological manifestation of the bilateral advantage was predicted, with strongest cortical activation for words in the bilateral condition. Critically, the memory circuit model predicts a significant interaction between lexicality (words vs. pseudowords) and presentation mode to emerge from physiological data (source strengths). The strongest hypothesis concerns the superiority of the bilateral condition over the best of the unilateral conditions (i.e., RVF for lexical stimuli), which would demonstrate a bilateral redundancy gain. 2. Methods and material 2.1. Participants Fifteen healthy participants (7 females; mean age: 23.9; education 12.6 years) were paid for their study participation. All subjects were native speakers of German and right-handed as verified by a modified version of the Edinburgh handedness questionnaire (Oldfield, 1971) (handedness quotient: 96.0). None of the participants had a history of neurological or psychopathological disorders. Subjects had normal or corrected to normal vision. This study was approved by the ethics committee of the University of Konstanz, Germany, where all data were collected. The study followed the ethical standards laid down in the 1964 Declaration of Helsinki. All participants gave informed consent prior to inclusion in the study.

2.2. Procedure In a lexical decision task, participants were instructed to decide whether a visually presented letter string was a meaningful German word or a meaningless pseudoword by bimanually pressing two out of four response buttons. In case of word presentation a response with both index fingers was required and in case of pseudoword presentation, a button press with both middle fingers should be executed. Subjects were instructed to respond as fast and as accurately as possible. During the whole experimental block subjects were requested to fixate their eyes on a fixation cross in the middle of a computer screen. Stimuli were presented tachistoscopically for 150 ms either unilaterally to the RVF or to the LVF or simultaneously to both visual fields (BVF). The interstimulus-interval (ISI) varied between 2.5 and 3.5 s. A 60 trials practice block preceded the experiment. The experiment comprised 240 stimuli (120 words and 120 pseudowords), which were presented in pseudo-randomized order. Each item occurred only once during the experiment. The duration of the experimental session was approximately 30 min.

2.3. Stimuli Words and pseudowords were presented in black upper-case letters on a grey background to reduce visual afterimages. All stimuli were bisyllabic and were four to eight letters long. Words were German content words with a high frequency of occurrence (100–1000 occurrences per 1 million words, according to Ortmann, 1995). Pseudowords were obtained either by permutation of letters within words or by exchanging letters between word stimuli. Pseudowords were pronounceable and orthographically regular but not homophonous to real words. It was ascertained that none of the pseudowords contained a real word.

2.4. Apparatus Stimuli were presented on a 17-in. monitor of an IBM compatible Pentium PC placed at a distance of 1 m in front of the participants. Stimuli appeared between 1.5◦ and 4.5◦ of horizontal and 0.6◦ of vertical visual angle. During the experiment, all participants had their chins in a chin rest with a forehead

B. Mohr et al. / Neuropsychologia 45 (2007) 2114–2124 restraint bar centered relative to the viewing screen. Two keypads each comprising two easily manageable micro switches served for response collection and were positioned on a table in front of the subject.

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Means in each window were compared by analyses of variance (ANOVA) with the factors Lexicality (Words vs. Pseudowords), Presentation Mode (LVF, BVF vs. RVF), Hemisphere (LH vs. RH) and Gradient (frontal, fronto-temporal, temporo-parietal and parieto-occipital).

2.5. Data acquisition and ERP analysis 2.6. Source estimation using minimum norm analysis The EEG (electroencephalogram) and EOG (electrooculogram) were recorded continuously with two 32-channel DC-amplifiers (SYNAMPS, Neuroscan) from 65 electrodes mounted on a cap referenced to Cz (Electrocap Inc.) using an equidistant electrode position system. Data were recorded with a bandpass of DC to 30 Hz and a sampling rate of 200 Hz. Impedances were kept below 5 k. Data were recorded continuously and stored for off-line analysis. After the experimental session, electrode positions were digitized using a 3D digitizer (Polhemus Inc.). Vertical, horizontal and blink electrooculograms (EOG) were recorded for later artifact correction following the MSEC (multiple source eye correction) method (Berg & Scherg, 1994). Additionally, trials were visually inspected. Only artifact free trials with correct responses performed within 2 s after stimulus onset were analyzed (72.9 percent, SD = 11.3, of all trials were included in data analysis). ERP data were averaged separately for each of the six conditions (words, pseudowords presented to the LVF, RVF and BVF) and filtered with a 20 Hz low pass filter. A baseline correction was performed for each individual and each condition by subtracting the average scalp distribution during a 200 ms epoch prior to stimulus onset from each data point. After average referencing the ERPs, variability of the electrode positions was reduced by spline-interpolation of the data from individually digitized electrode positions on a standardized electrode montage. For statistical analysis of ERP data, data were normalized by calculating z-values across all subjects (McCarthy & Wood, 1985). The bilateral advantage was analyzed by comparing the bilateral condition (BVF) with both unilateral conditions (RVF and LVF). In order to localize the bilateral advantage in a temporal and topographical way, we performed statistical analysis on behavioral data, evoked potential data and on the minimum norm solution. Behavioral data (accuracy and latency) were analyzed by ANOVAs with the factors Lexicality (words vs. pseudowords) and Presentation Mode (LVF, RVF vs. BVF). For analyzing the event-related potential (ERP) data, head positions of the electrodes were combined into four electrode arrays (each comprising mean amplitude of three electrodes) within each hemisphere: frontal, fronto-temporal, temporo-parietal and parieto-occipital. Mean amplitudes for each electrode array were determined for words and pseudowords in the three presentation conditions (LVF, RVF and BVF). Fig. 1 shows root mean square (RMS) curves for all six experimental conditions. As the latency of the RMS peak was consistent with prediction and with previous research (see Section 1), a time window from 160 to 200 ms after stimulus onset was selected for the critical statistical analysis of the bilateral advantage. To make sure that we did not miss critical effects elsewhere, the interval 40–200 ms post stimulus onset was sliced into 40 ms windows and each submitted to a separate analysis. Later ERPs were analyzed in the window 200–400 ms. Note that the selection of time windows of different widths is justified by the shape of the ERP curves, which first exhibit a sharp and later-on shows slowly changing dynamics.

ERP data are difficult to interpret in terms of neuronal generators. Sources that are tangentially oriented to the scalp produce their peaks of activity at considerable distances from the true source location. If multiple sources are active, their potential distributions are likely to interfere with each other, such that the contributions from particular sources cannot be discerned. Source analysis in general attempts to deal with this problem. Various algorithms, incorporating different kinds of modeling assumptions, have been suggested (Baillet, Mosher, & Leahy, 2001; Fuchs, Wagner, Kohler, & Wischmann, 1999; Michel et al., 2004). If the source distribution can be expected to be complex (as for cognitive ERP components) and if the signal-to-noise ratio is low (as for single subject data), a method relying on minimal modeling assumptions is recommended. Such a method is the classical minimum L2-norm (MN) method (Grave de Peralta, Hauk, Gonzalez Andino, Vogt, & Michel, 1997; Hamalainen & Ilmoniemi, 1994). It is capable of producing a two-dimensional blurred version of the real source distribution, even if the signal-to-noise ratio is low (Hauk, Keil, Elbert, & Mueller, 2002). The method can therefore be applied to individual subject data, which in turn can be submitted to statistical analysis. The implementation of the MN method used in this experiment follows the suggestions of Hauk et al. (2002). Because current sources can be distributed in the whole brain volume, initially a three-dimensional source space was chosen. It consisted of 1,655 dipolar current sources distributed over four concentric shells with radii 0.8, 0.6, 0.4 and 0.2, respectively (electrodes at radius 1). The MN method always produces maximal amplitudes on the outermost shell. However, the deeper the shell, the lower the spatial resolution, but the higher the relative sensitivity to deeper current sources. As a compromise between these two aspects and for data reduction we chose the shell with radius 0.6 for further analysis. The influence of noise on MN estimates can be controlled by imposing a certain degree of smoothness. This was accomplished by Tikhonov regularization, which is optimal for suppressing spatially uncorrelated noise, such that the mean residual variance of our estimates over all data sets was 5 percent (Bertero, de Mol, & Pike, 1988). The method applied in this study is a source estimation technique, which does not require a priori assumptions on location and number of dipoles. The minimum norm (MN, L2-norm) estimates were computed separately for conditions and subjects according to Hauk et al. (2002). Six dipole arrays were selected, each containing a number of sources over anterior, medial and posterior areas of the right and left hemisphere. The same time window from 160 to 200 ms as for ERP-analysis was chosen. Local source strengths from the Minimum Norm Estimation were analyzed in a factorial design. This was done by computing ANOVAs with the factors Lexicality (words vs. pseudowords), Presentation Mode (LVF, BVF vs. RVF), Gradient (frontal, temporal vs. parietal) and Hemisphere (left vs. right). For all analyses, p-values were corrected with Greenhouse-Geisser procedure, when appropriate (if df > 1). Significant interac-

Fig. 1. Root mean square values (RMS) of ERP amplitudes calculated from all recording electrodes for words and pseudowords presented in the LVF, RVF and both visual fields (BVF) are displayed as a function of time after stimulus presentation onset. Please note the early peak before 200 ms.

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tions were further analyzed by planned comparisons using one-way ANOVAs. For statistical analysis, source locations that were exactly below the recording electrodes and approximately at the level of the cortical surface were chosen. As it is known where on the cortical surface the 10/20 and 10/10 electrode locations project (Lagerlund et al., 1994), the source loci can be specified in terms of gyri and sulci, or in terms of Talairach coordinates (Talairach & Tournoux, 1988). Thus, we used the published correspondence between projections of 10/10 electrode loci and anatomical landmarks (e.g., superior temporal gyrus) in a large sample of brains as a reference when drawing any conclusion on source locations.

3. Results 3.1. Behavioral data: accuracy and latency Overall accuracy was higher for pseudowords than for words (Lexicality F(1, 14) = 10.42, p < .01), as demonstrated in Fig. 2A. A significant main effect of the factor Presentation Mode showed that performance was highest in the bilateral condition and lowest in the LVF condition (Presentation Mode: F(1, 14) = 33.02, p < .001). A significant Lexicality (words vs. pseudowords) × Presentation Mode (LVF, BVF vs. RVF) interaction was obtained (F(2, 28) = 24.28, ε = 0.89, p < .001). Planned comparisons revealed a right visual field advantage (RVFA) for words (F(1, 14) = 12.74, p < .01). As a bilateral advantage or bilateral redundancy gain is reflected in a superior performance in the bilateral condition in comparison to the best unilateral condition, the crucial comparison is between BVF and RVF con-

dition in which stimuli are delivered to the language-dominant left hemisphere (stimulation via the RVF) alone. Behavioral data showed a bilateral advantage for words (BVF vs. LVF: F(1, 14) = 45.97, p < .001; BVF vs. RVF: F(1, 14) = 76.00, p < .001). No bilateral advantage for pseudowords was found. In addition to accuracy data analysis, an analysis of d values was performed as a measure of the subjects’ ability to discriminate words from pseudowords. Hits were determined as the percentage of correct word decisions when a word was presented. False alarms were determined as the percentage of incorrect word decisions when a pseudoword was presented. Word detection was best when stimuli were presented bilaterally (d = 2.07), second best in the RVF condition (d = 1.84) and worst under LVF presentation (d = 1.38). This difference was reflected in a clearly significant main effect of Presentation Mode, F(2, 28) = 31.8, p < .0001, with significant differences between any two of the three presentation conditions (LVF vs. RVF: F(1, 14) = 20.08, p < .0004; LVF vs. BVF: F(1, 14) = 40.17, p < .00002; RVF vs. BVF: F(1, 16) = 45,12, p < .00001). These data add to and further strengthen the behavioral evidence for the bilateral advantage in lexical processing. Latencies of correct responses are displayed in Fig. 2B. A significant main effect of the factor Presentation Mode (F(1, 14) = 19.92, p < .001) indicated slowest reaction times after stimulus presentation in the LVF and fastest responses after bilateral presentation. The marginally significant main effect for Lexicality (F(1, 14) = 3.23, p < .1) was explained by overall faster reactions for words than for pseudowords. Response times also revealed a significant Lexicality × Presentation Mode interaction (F(1, 14) = 20.76, p < .001). Planned comparisons once again showed a right visual field advantage for words and pseudowords (words: F(1, 14) = 12.15, p < .01; pseudowords: F(1, 14) = 8.91, p < .01). Crucially, there was also a bilateral advantage specifically for words, with faster responses in the bilateral condition relative to both unilateral conditions (BVF vs. RVF: F(1, 14) = 50.77, p < .001; BVF vs. LVF: F(1, 14) = 39.43, p < .001). In the bilateral condition, faster responses were obtained for words than for pseudowords (F(1, 14) = 25.42, p < .001). The higher rate of misses for words in the RVF and especially the LVF condition may reflect a general tendency of our subjects to make the pseudoword judgement in case of uncertainty. 3.2. Event-related potential data

Fig. 2. Behavioral data: Mean (standard errors indicated as bars) percentage of correct responses (A) and mean reaction times (B) are displayed for the presentation conditions (LVF, BVF and RVF), and for words and pseudowords. A bilateral advantage was revealed for words, but not for pseudowords, by both accuracy and latency data.

A time window between 160 and 200 ms post stimulus onset was selected for statistical analysis because earlier data had shown early neurophysiological indicators of lexicality effects, or “wordness”, in this time range (e.g., Hauk & Pulverm¨uller, 2004; Pulverm¨uller et al., 1999). The RMS curves confirmed this also for the present study: the earliest differences arose at 160–200 ms (see Fig. 1). ERP amplitudes and topographies for words and pseudowords showed pronounced differences among the three Presentation Modes (Fig. 3A and B). A summary of all significant main effects and interactions obtained in the ERP analysis of all visual field conditions is given in Table 1. Most importantly, there was a significant interac-

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Fig. 3. Grand average ERP topographies (all average reference) of words and pseudowords presented in the LVF, RVF and BVF in the time window 160–200 ms after stimulus onset (A). Topographies of the difference BVF minus RVF (B) for words and pseudowords, as well as the difference between words and pseudowords in the time window 160–200 ms after stimulus onset are displayed. This difference is distributed over both hemispheres.

tion between Lexicality and Presentation Mode (F(2, 28) = 3.40, ε = 0.04, p = .05), indicating increased amplitudes for words, particularly in the bilateral condition. Planned comparisons for this interaction showed that the mean ERP amplitude for words after bilateral stimulation was more negative than for pseudowords (F(1, 14) = 15.00, p < .001). Fig. 4 depicts mean amplitudes of response to words and pseudowords as a function of presentation mode and hemisphere. Neither Lexicality nor Presentation Mode significantly

interacted with any of the topographic factors of Gradient or Hemisphere. Planned comparisons revealed a significant difference for words only between the BVF and RVF condition (F(1, 14) = 14.87, p < .001). Analyses calculated for the second peak, around 300–400 ms post stimulus onset, did not yield any significant interactions or effects of lexicality. Systematic check of 40 ms windows up to 200 ms also failed to demonstrate significant changes with lexicality or an interaction involving this factor.

Table 1 A summary of significant main effects and interactions obtained in ERP (A) and MNE (B) analysis is presented Factors

F

GG-ε

p

(A) ERPs: comparisons of LVF, RVF and BVF conditions Lexicality Gradient Presentation Mode × Gradient Presentation Mode × Hemisphere Presentation Mode × Lexicality

F(1, 14) = 10.77 F(3, 42) = 3.81 F(6, 84) = 23.60 F(2, 28) = 27.46 F(2, 28) = 3.40

1.00 0.44 0.29 0.63 0.04

<.01 <.055 <.001 <.001 <.05

(B) MNEs: comparisons of LVF, RVF and BVF conditions Presentation Mode Gradient Gradient × Hemisphere Gradient × Lexicality Presentation Mode × Hemisphere Lexicality × Gradient × Hemisphere Gradient × Hemisphere × Lexicality × Presentation Mode

F(2, 28) = 5.21 F(2, 28) = 16.57 F(2, 28) = 4.89 F(2, 28) = 3.33 F(2, 28) = 6.90 F(2, 28) = 4.00 F(4, 56) = 4.99

0.78 0.52 0.55 0.63 0.62 0.61 0.001

<.03 <.01 <.04 <.05 <.02 <.055 <.01

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Fig. 4. ERP data: Mean amplitudes (in ␮V, standard errors indicated as bars) in the time range from 160 to 200 ms are provided separately for the presentation conditions (LVF, BVF, and RVF), words and pseudowords, and hemispheres (LH and RH). In the bilateral condition (BVF), larger negativities for words than for pseudowords were observed over both hemispheres.

3.3. ERP source analysis: minimum norm estimates Our main interest in this study was to specify focal brain activation and their relationship to lexicality and presentation modes. Therefore, minimum norm source estimations were calculated. This was done separately for each subject, condition, and for words and pseudowords in the time window from 160 to 200 ms and averaged across subjects (see Fig. 5A). In addition, the difference in source estimations between BVF and RVF conditions (Fig. 5B) is displayed. In the unilateral conditions, activation peaked at posterior regions of the respective contralateral hemisphere. Source estimation indicated a bilateral

distribution of activity, which tended to be stronger in the left hemisphere than in the right, after stimulus presentation in both visual fields. However, activation in right parieto-occipital areas was stronger in the bilateral condition compared with the RVF condition for both words and pseudowords. BVF-induced activation for words was only present in left temporal regions. A four-way ANOVA including the factors Lexicality, Presentation Mode, Laterality and Gradient was performed on the minimum norm estimations obtained from the 160–200 ms time window where significant ERP effects became manifest. There was a significant main effect of Gradient F(2, 28) = 16.57, ε = 0.52, p < .01 showing strongest cortical sources in parietal cortical areas and a significant main effect of Presentation Mode F(2, 28) = 5.21, ε = 0.78, p < .03) indicating strongest cortical activation in the bilateral condition. No hemispheric difference emerged in the bilateral condition, but otherwise the expected laterality was significant (Presentation Mode × Hemisphere F(2, 28) = 6.90, ε = 0.62, p < .02). Laterality varied with electrode site (Gradient × Hemisphere F(2, 28) = 4.89, ε = 0.55, p < .04): at frontal regions activity was lateralized to the right; activity at parietal sites was lateralized to the left. The laterality effect tended to be more pronounced for words than for pseudowords (Lexicality × Gradient: F(2, 28) = 3.33, ε = 0.63, p = .077; Lexicality × Gradient × Hemisphere: F(2, 28) = 4.00, ε = 0.61, p = .055). Critically, source analysis revealed a significant Lexicality × Presentation Mode × Hemisphere × Gradient interaction (F(4, 56) = 4.99, ε = 0.001, p < .01) due to increased cortical

Fig. 5. Grand mean topographies of source distributions estimated by the minimum norm solution are displayed. Topographies for words and pseudowords in the three conditions (LVF, BVF and RVF) in the time window 160–200 ms are presented (A). Dark areas represent regions of increased source activity. (B) Contrasts topographies of difference source distributions of the neurophysiological correlate of the bilateral redundancy effect (BVF minus RVF) for words and pseudowords and shows the differential bilateral redundant target effect (RTE for words minus RTE for pseudowords (B, figure on the right). Dark areas represent regions of increased electrocortical activity after BVF stimulation and light areas represent higher electrocortical activity after RVF stimulation.

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Fig. 6. Dynamics of cortical source estimations critical for the redundant target effect for words but not pseudowords: Mean minimum norm estimates (in nA/cm2 , standard errors indicated in bars) in the time range from 160 to 200 ms are displayed for temporal sources. There was significantly higher activation, relative to both unilateral conditions, for words in both hemispheres. Activation for pseudowords after bilateral stimulation was only increased compared with unilateral stimulation in the respective ipsilateral hemisphere.

activity after bilateral stimulation relative to both unilateral conditions for words, an absence or reduction of this effect for pseudowords and a focal specificity of all this in temporal cortex. This critical interaction is displayed in Fig. 6. Analyses carried out for earlier and later time windows did not yield any significant interaction involving the factors Lexicality and Presentation Mode. Planned comparison F-tests were performed to investigate this complex four-way interaction and to address the critical questions of this experiment: As temporal sources showed the differential effects most clearly, these tests focused on temporal regions in both hemispheres. In each hemisphere, direct stimulation with words in the contralateral visual hemi-field led to activation that was weaker than activation elicited by bilateral presentation. These critical comparisons are for activation in the left hemisphere between BVF and RVF conditions (in Fig. 6: bar 2 vs. bar 3 from the left) and for right hemispheric activation between BVF and LVF conditions (Fig. 6, bar 7 vs. bar 8). Both comparisons were significantly different from each other when word stimuli were processed (F-values > 4.8, p-values < .05, df1 = 1, df2 = 14). A corresponding effect was clearly absent for pseudowords (cf. Fig. 6: bars 5 and 6, and bars 10 and 11; F-values < 1). This activation enhancement for words must be due to the extra stimulation of the other hemisphere and therefore to incoming activation flow from that hemisphere. As this effect is only revealed for words but not for pseudowords, the cognitive differences between these stimulus types must be related to the effect. Fig. 6 also shows other effects: Ipsilateral stimulation always leads to less activation in a given hemisphere than contralateral or bilateral stimulation. This is a trivial effect related to the full crossing of visual fibers and argues in favor of the reliability of the source estimation procedure. Finally, the bilateral condition suggests that words tend to evoke stronger activation than pseudowords, but this difference could not be confirmed by data from individual presentation conditions.

Using a lexical decision task with visual presentation of stimuli, the lexicality-related bilateral advantage known from behavioral studies of words presented in the visual half-fields was replicated, both in accuracy data and latencies. Words, but not pseudowords, were processed more rapidly and more reliably when being presented in a redundant fashion with two identical copies in the left and right visual hemi-fields. For the first time, however, we were able to demonstrate a neurophysiological correlate of the bilateral gain specific to visually presented words: Words, but not pseudowords, elicited significantly greater ERPs when presented in the bilateral mode compared with the best unilateral stimulation (RVF). Source analysis showed that stronger cortical generator activation was present in this case, possibly reflecting activation of interhemispheric cortical memory circuits representing and processing words. A similar analysis for pseudowords failed to reveal a comparable physiological benefit from redundant stimulation, thus yielding a significant interaction of the lexicality (word vs. pseudoword) and presentation mode variables. The effect was apparent at 160–200 ms after stimulus onset, and the source estimates indicated that bihemispheric temporal foci in the posterior part of the perisylvian area made a main contribution to the neurophysiological processes underlying the bilateral redundancy gain. 4.1. Replicating the word-specific bilateral redundancy gain Behavioral lexical decision responses to words and pseudowords were compared between the left visual field, the right visual field and the bilateral stimulation condition. In the latter, two copies of a stimulus were presented simultaneously in the LVF and RVF. Apart from a general right visual field advantage, bilateral stimulation led to faster and more accurate processing of words, an effect known as the word-specific bilateral redundancy gain. As the lexical bilateral advantage was absent for pseudowords, the overall pattern we obtained in behavioral data replicated previous findings (Mohr, Pulverm¨uller, & Zaidel, 1994; Mohr et al., 1996; Yoshizaki, 2001). Crucially, both response times and accuracy measures documented better behavioral performance when word stimuli were delivered in the redundant bilateral condition compared with the best unilateral condition. As there was also the commonly observed right visual field advantage for words, the better of the non-redundant unilateral conditions was the RVF presentation. Differential discrimination performance in the three presentation modes could also be confirmed by signal detection analysis using the d measure. The right visual field advantage is usually interpreted as evidence for a locus of language processing in the left hemisphere, although others and we have argued that it is equally compatible with a gradual difference. The dominant left hemisphere is better than the right hemisphere in processing word-related information, but this still allows for a role of both hemispheres in lexical processing (Pulverm¨uller & Mohr, 1996). The bilateral redundancy gain is evidence that delivering lexico-semantic

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information about meaningful words to both hemispheres simultaneously yields better processing than direct stimulation of the dominant hemisphere alone. This has been interpreted as support for a role of both hemispheres in language processing (Mohr, Pulverm¨uller, & Zaidel, 1994). We have also argued that race models of hemispheric processing, according to which both hemispheres each house a lexicon and the two compete in determining the lexical decision response, do not account for the evidence on word and pseudoword processing accumulated so far. In this case, the argument does not rest on super-additivity of behavioral performance in the BVF condition, which we did not observe here or in earlier experiments (for discussion, see Mohr et al., 1996), but on the stimulus-specificity of the gain. First, the absence of any bilateral redundancy gain for pseudowords is not explained straightforwardly by race models. Even if pseudowords are processed using a “time out” strategy, the redundant presentation should allow for a facilitation of perceptual processes, as bilateral redundancy gains have been reported for elementary stimuli such as gratings (for overview, see Miniussi et al., 1998). Because, similar to several earlier studies, the present data failed to hint towards a bilateral gain for pseudowords in the lexical decision task, we do not believe that race models provide a successful explanation for the present data. A second argument against such an approach comes from patient populations with defects in interhemispheric communication, including split brain patients and, for example, patients with schizophrenia. These have been shown not to exhibit a bilateral advantage for words, even if they show clear behavioral signatures of language specific processes, including, for example, a pronounced right visual field advantage and lefthemispheric laterality (Beaumont & Dimond, 1973; Endrass, Mohr, & Rockstroh, 2002; Mohr et al., 2000). The bilateral redundancy gain for words in behavior was found to be similar to the redundancy advantage for identical copies of words presented to the dominant hemisphere and significantly above the redundancy effect seen with LVF presentation (Mohr et al., 1996). This suggests that facilitatory connections in lexical circuits are as effective between the hemispheres as they are within the dominant hemisphere. The lexical bilateral redundancy gain appears to be best explained by a model of cooperative interhemispheric interaction where information about a word from both hemi-fields is integrated. In neurobiological terms, interhemispheric neuron ensembles, which process perceptual and linguistic features of a word, could provide the substrate for summation of neuronal activity across hemispheres and therefore accumulation of evidence from both visual hemi-fields (Mohr & Pulverm¨uller, 2002; Shillcock, Ellison, & Monaghan, 2000). Bilateral stimulation of feature information for words would therefore activate neurons in both hemispheres leading to neuronal summation processes and therefore to faster and more reliable ignition of the entire cell assembly, which is experienced and measured as a faster perception and processing of the stimulus. The idea of bilateral interhemispheric networks underlying lexico-semantic processing is also in agreement with a range of neuroimaging and neuropsychological observations (Pulverm¨uller, 2005). It is also in agreement with other redundant target effects seen for familiar

stimuli eliciting higher cognitive processes, especially familiar faces, and its absence for matched unfamiliar faces (Mohr et al., 2002). 4.2. ERP and source correlates of the lexical bilateral redundancy gain This study investigated the neurophysiological basis of the bilateral redundancy gain for written words. Event-related potential data revealed a significant Lexicality × Presentation Mode interaction. Bilaterally presented words elicited a greater negativity than pseudowords in the bilateral condition in the time window from 160 to 200 ms. Negativity for words differed significantly only between the bilateral and RVF condition. Over both hemispheres, bilaterally presented words were more negative than words presented to the RVF. In contrast, pseudowords differed only over the right hemisphere. Source analysis revealed a topographically specific correlate for the bilateral advantage. The significant Lexicality × Presentation Mode × Gradient × Hemisphere interaction suggested a contribution of left-temporal regions to the bilateral gain. In both hemispheres, especially in temporal lobes, bilaterally presented words elicited stronger activation than each of the unilateral conditions did. Irrespective of the nature of the stimulus (word or pseudoword), bilateral presentation elicited stronger activation than ipsilateral visual stimulation alone (Fig. 6). Thus, enhanced word-elicited activation at temporal sites of each hemisphere in the bilateral condition compared with the contralateral visual field appears to be the cortical signature of the bilateral advantage, which is absent for unfamiliar pseudowords precisely matched to the word stimuli. 4.3. Multiple bilateral gains The present data revealed a bilateral redundancy gain for words but not for pseudowords in the lexical decision task. This is consistent with earlier findings, where pseudowords, but also other unfamiliar stimuli such as unfamiliar faces, failed to elicit any processing benefit from redundant stimulation (e.g., Mohr et al., 2002; Schweinberger et al., 2003). This pattern of results has given rise to the idea that the bilateral redundancy gain is specific to learned and familiar meaningful stimuli, but is entirely absent for unfamiliar ones that are not meaningful in an abstract cognitive sense. It must, however, be mentioned (see also Section 1), that a whole literature exists on bilateral redundancy gains elicited by elementary stimuli, including bars and grids (Miniussi et al., 1998). Some studies have reported redundancy gains for cvc-nonwords, although these gains were significantly reduced compared with those to matched word stimuli. This range of facts suggests that redundancy gains can be observed at different levels, at the level of elementary visual stimulus perception (Corballis, 1998; Savazzi & Marzi, 2004), at the level of motor control (Iacoboni & Zaidel, 2003; Roser & Corballis, 2003), but also at the higher cognitive level. At the higher cognitive level, familiarity and the frequency with which stimuli have been perceived in the past (during learning processes) appears to be critical for determining the strength of the bilateral gain.

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Also, task factors may play a role. For example, the lexical decision task may bias the results in favor of a cognitive bilateral advantage. In contrast, a recognition or memory task that can be solved by focussing on more elementary stimulus features may remove this bias and therefore allow redundancy gains at perceptual and motor levels to overlay the higher cognitive effects. A strong claim should probably not be based on the absence of a bilateral gain for any stimulus category, but on the increase in bilateral gain for one stimulus category compared with a well-matched control. In this sense, the “word-specific bilateral gain” or the “familiar face-specific bilateral gain” would denote the additional increase in redundancy gain achieved by familiar stimuli compared with their matched unfamiliar ones, that is, the surplus documented by the significant interaction of the factors Lexicality × Presentation Mode. 4.4. Mechanisms of the bilateral redundancy gain for learned meaningful materials A significant interaction demonstrated that source strengths in the temporal cortex of both hemispheres were significantly increased for bilateral redundant word presentation (relative to either of the unilateral conditions), and that this was not the case for pseudowords. The data suggest that the mechanisms underlying the bilateral redundancy gain may be localized in the temporal cortex of both hemispheres. If stimulation is unilateral, the contralateral temporal cortex appears to be activated but if there is bilateral stimulation with words, the activation in both temporal cortices is stronger compared to the strong contralateral activation achieved in the unilateral conditions. This is evidence that summation from the respective other hemisphere kicks in at these loci. Theoretically, strongly interconnected neuronal assemblies distributed over large parts of the cortex can explain the bilateral redundancy gain. For learned meaningful words, these neuronal assemblies have been proposed to be mainly localized in left hemispheric cortex, although an additional participation of neurons in the right (non-dominant) cortex has been claimed on the basis of evidence for right-hemispheric language mechanisms (Pulverm¨uller & Mohr, 1996). We may therefore say that the neuron density of a word-related cell assembly is higher in left temporal cortex compared with the homotopic areas on the right. However, as each neuron in the assembly is the target of axons from multiple other neurons belonging to the same assembly, it can be the basis of processes of neuronal summation. It is this neuronal summation mediated by interhemispheric connections that we propose as the mechanism underlying the bilateral redundancy gain. In an earlier behavioral study, we estimated the time at which a word-related left-hemispheric (perisylvian) network is activated by a written word stimulus to be at around 150 ms after stimulation onset (Mohr & Pulverm¨uller, 2002). Neurophysiological evidence is consistent with this: Words and pseudowords as well as words from different lexico-semantic categories first differ neurophysiologically in the N160 component (or a late part of the N100) and the Mismatch Negativity (latency 130–200 ms after point of word recognition) (Pulverm¨uller et al., 1995, 2001;

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Pulverm¨uller, 2007; Sereno, Rayner, & Posner, 1998). This indicates that the neurophysiological mechanisms specific to lexical and semantic processing take place at a latency of 150–200 ms. The present finding of the rather early latency of the bilateral redundancy gain specific to words further strengthens the view that lexical processes are reflected at the neurophysiological level within the first 200 ms after lexical information comes in. It is at this early latency where the summation processes within cortical cell assemblies may first occur. Acknowledgements We would like to thank two anonymous referees for their comments and suggestions and Gabriele Geiger and Katja Hannemann for help in conducting the experiment. This study was supported by grants of the Deutsche Forschungsgemeinschaft (Mo 697/1-1, Mo 697/2-1 and Ro 805/11-1). References Baillet, S., Mosher, J. C., & Leahy, R. M. (2001). Electromagnetic brain mapping. IEEE Signal Processing Magazine, 18, 14–30. Banich, M., & Karol, D. L. (1992). The sum of the parts does not equal the whole: Evidence from bihemispheric processing. Journal of Experimental Psychology: Human Perception and Performance, 18, 763–784. Beaumont, J. G., & Dimond, S. (1973). Brain disconnection and schizophrenia. British Journal of Psychiatry, 123, 661–662. Begleiter, H., & Platz, A. (1969). Cortical evoked potentials to semantic stimuli. Psychophysiology, 6, 91–100. Berg, P., & Scherg, M. (1994). A multiple source approach to the correction of eye artifacts. Electroencephalography and Clinical Neurophysiology, 90, 229–241. Bernat, E., Bunce, S., & Shevrin, H. (2001). Event-related brain potentials differentiate positive and negative mood adjectives during both supraliminal and subliminal visual processing. International Journal of Psychophysiology, 42, 11–34. Bertero, M., de Mol, C., & Pike, E. R. (1988). Linear inverse problems with discrete data. II. Stability and regularisation. Inverse Problems, 4, 573–594. Brown, W. S., & Jeeves, M. A. (1999). Bilateral visual field processing and evoked potential interhemispheric transmission time. Neuropsychologia, 31, 1267–1281. Brown, W. S., Larson, E. B., & Jeeves, M. A. (1994). Directional asymmetries in interhemispheric transmission time: Evidence from visual evoked potentials. Neuropsychologia, 32, 439–448. Compton, P. E., Grossenbacher, P., Posner, M. I., & Tucker, D. M. (1991). A cognitive-anatomical approach to attention in lexical access. Journal of Cognitive Neuroscience, 3, 304–312. Corballis, M. C. (1998). Interhemispheric neural summation in the absence of the corpus callosum. Brain, 121, 1795–1807. Endrass, T., Mohr, B., & Pulverm¨uller, F. (2004). Enhanced mismatch negativity brain response after binaural word presentation. European Journal of Neuroscience, 19, 1653–1660. Endrass, T., Mohr, B., & Rockstroh, B. (2002). Reduced interhemispheric transmission in schizophrenia patients: Evidence from event-related potentials. Neuroscience Letters, 320, 57–60. Fuchs, M., Wagner, M., Kohler, T., & Wischmann, H. A. (1999). Linear and nonlinear current density reconstructions. Journal of Clinical Neurophysiology, 16, 267–295. Grave de Peralta, R., Hauk, O., Gonzalez Andino, S., Vogt, H., & Michel, C. (1997). Linear inverse solutions with optimal resolution kernels applied to electromagnetic tomography. Human Brain Mapping, 5, 454–467. Hamalainen, M. S., & Ilmoniemi, R. J. (1994). Interpreting magnetic fields of the brain: Minimum norm estimates. Medical & Biological Engineering & Computing, 32, 35–42.

2124

B. Mohr et al. / Neuropsychologia 45 (2007) 2114–2124

Hasbrooke, R. E., & Chiarello, C. (1998). Bihemispheric processing of redundant bilateral lexical information. Neuropsychology, 12, 78–94. Hauk, O., Davis, M. H., Ford, M., Pulverm¨uller, F., & Marslen-Wilson, W. D. (2006). The time course of visual word recognition as revealed by linear regression analysis of ERP data. Neuroimage, 30(4), 1383–1400. Hauk, O., Keil, A., Elbert, T., & Mueller, M. M. (2002). Comparison of data transformation procedures to enhance topographical accuracy in time-series analysis of the human EEG. Journal of Neuroscience Methods, 113–122. Hauk, O., Patterson, K., Woollam, A., Watling, L., Pulverm¨uller, F., & Rogers, T. T. (2006). [Q:] When would you prefer a SOSSAGE to a SAUSAGE? [A:] At about 100 ms. ERP correlates of orthographic typicality and lexicality in written word recognition. Journal of Cognitive Neuroscience, 18, 818–832. Hauk, O., & Pulverm¨uller, F. (2004). Effects of word length and frequency on the human event-related potential. Clinical Neurophysiology, 115, 1090–1103. Hebb, D. (1949). The organization of behavior. A neuropsychological theory. New York: Wiley. Hellige, J. B., Taylor, A. K., & Eng, T. L. (1989). Interhemispheric interaction when both hemispheres have access to the same stimulus information. Journal of Experimental Psychology: Human Perception and Performance, 15, 711–722. Iacoboni, M., & Zaidel, E. (2003). Interhemispheric visuo-motor integration in humans: The effect of redundant targets. European Journal of Neuroscience, 17(9), 1981–1986. Lagerlund, T. D., Sharbrough, F. W., Jack, C. R., Jr., Erickson, B. J., Strelow, D. C., Cicora, K. M., et al. (1994). Determination of 10-20 system electrode locations using magnetic resonance scanning with markers. Electroencephalography and Clinical Neurophysiology, 86, 7–14. Marks, N. L., & Hellige, J. B. (1999). Effects of bilateral stimulation and stimulus redundancy on interhemispheric interaction. Neuropsychology, 13, 475–487. Marks, N. L., & Hellige, J. B. (2003). Interhemispheric interaction in bilateral redundancy gain: Effects of stimulus format. Neuropsychology, 17, 578–593. McCarthy, G., & Wood, C. (1985). Scalp distributions of event-related potential: An ambiguity associated with analysis of variance models. Electroencephalography and Clinical Neurophysiology, 62, 203–208. Michel, C., Murray, M. M., Lantz, G., Gonzalez, S., Spinelli, L., & Grave De Peralta, R. (2004). EEG source imaging. Clinical Neurophysiology, 115, 2195–2222. Miller, J. (1982). Divided attention: Evidence for coactivation with redundant signals. Cognitive Psychology, 14, 247–279. Miniussi, C., Girelli, M., & Marzi, C. A. (1998). Neural site of the redundant target effect: Electrophysiological evidence. Journal of Cognitive Neuroscience, 10, 216–230. Mohr, B., Landgrebe, A., & Schweinberger, S. (2002). Interhemispheric cooperation for familiar but not unfamiliar face processing. Neuropsychologia, 40, 1841–1848. Mohr, B., & Pulverm¨uller, F. (2002). Redundancy gains and costs in cognitive processing: Effects of short stimulus onset asynchronies. Journal of Experimental Psychology: Learning, Memory and Cognition, 28, 1200–1223. Mohr, B., Pulverm¨uller, F., Cohen, R., & Rockstroh, B. (2000). Interhemispheric cooperation during word processing: Evidence for callosal transfer dysfunction in schizophrenic patients. Schizophrenia Research, 46, 231–239. Mohr, B., Pulverm¨uller, F., Mittelst¨adt, K., & Rayman, J. (1996). Multiple simultaneous stimulus presentation facilitates lexical processing. Neuropsychologia, 34, 1003–1013. Mohr, B., Pulverm¨uller, F., Rayman, J., & Zaidel, E. (1994). Interhemispheric cooperation during lexical processing is mediated by the corpus callosum: Evidence from the split-brain. Neuroscience Letters, 181, 17–21. Mohr, B., Pulverm¨uller, F., & Zaidel, E. (1994). Lexical decision after left, right, and bilateral presentation of content words, function words, and nonwords: Evidence for interhemispheric interaction. Neuropsychologia, 32, 105–124.

Murray, M. M., Foxe, J. J., Higgins, B. A., Javitt, D. C., & Schroeder, C. E. (2001). Visuo-spatial neural response interactions in early cortical processing during a simple reaction time task: A high-density electrical mapping study. Neuropsychologia, 39, 828–844. Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113. Ortigue, S., Michel, C. M., Murray, M., Mohr, C., Carbonnel, S., & Landis, T. (2004). Electrical neuroimaging reveals early generator modulation to emotional words. Neuroimage, 21, 1242–1251. Ortmann, W. D. (1995). Hochfrequente deutsche Wortformen. Bd. 1 & 2. M¨unchen: Goethe-Institut, Arbeitsstelle f¨ur wissenschaftliche Didaktik. Pulverm¨uller, F. (1999). Words in the brain’s language. Behavioural and Brain Sciences, 22, 253–336. Pulverm¨uller, F. (2005). Brain mechanisms linking language and action. Nature Reviews Neuroscience, 6(7), 576–582. Pulverm¨uller, F. (2007). Word processing in the brain as revealed by neurophysiological imaging using EEG and MEG. In G. Gaskell (Ed.), Handbook of psycholinguistics. Oxford: Oxford University Press (in press). Pulverm¨uller, F., Kujala, T., Shtyrov, Y., Simola, J., Tiitinen, H., Alku, P., et al. (2001). Memory traces for words as revealed by the Mismatch Negativity (MMN). NeuroImage, 14, 107–616. Pulverm¨uller, F., Lutzenberger, W., & Birbaumer, N. (1995). Electrocortical distinction of vocabulary types. Electroencephalography and Clinical Neurophysiology, 94, 357–370. Pulverm¨uller, F., Lutzenberger, W., & Preissl, H. (1999). Nouns and verbs in the intact brain: Evidence from event-related potentials and high-frequency cortical responses. Cerebral Cortex, 9(5), 497–506. Pulverm¨uller, F., & Mohr, B. (1996). The concept of transcortical cell assemblies: A key to the understanding of cortical lateralization and interhemispheric interaction. Neuroscience and Biobehavioural Reviews, 20, 557–566. Pulverm¨uller, F., & Shtyrov, Y. (2003). Automatic processing of grammar in the human brain as revealed by the mismatch negativity. NeuroImage, 20, 159–172. Reuter-Lorenz, P. A., Nozawa, G., Gazzaniga, M. S., & Hughes, H. C. (1995). Fate of neglected targets: A chronometric analysis of redundant target effects in the bisected brain. Journal of Experimental Psychology: Human Perception and Performance, 21(2), 211–230. Roser, M., & Corballis, M. C. (2003). Interhemispheric neural summation in the split brain: Effects of stimulus colour and task. Neuropsychologia, 41, 830–846. Savazzi, S., & Marzi, C. A. (2004). The superior colliculus subserves interhemispheric neural summation in both normals and patients with a total section or agenesis of the corpus callosum. Neuropsychologia, 42(12), 1608–1618. Schweinberger, S. R., Landgrebe, A., Mohr, B., & Kaufmann, J. M. (2003). Personal names and the human right hemisphere: An illusory link? Brain and Language, 18, 111–120. Sereno, S. C., Rayner, K., & Posner, M. I. (1998). Establishing a time line for word recognition: Evidence from eye movements and event-related potentials. NeuroReport, 13, 2195–2200. Shillcock, R., Ellison, T. M., & Monaghan, P. (2000). Eye-fixation behaviour, lexical storage, and visual word recognition in a split processing model. Psychological Review, 107, 824–851. Shtyrov, J., & Pulverm¨uller, F. (2002). Neurophysiological evidence of memory traces for words in the human brain. Neuroreport, 13, 521–525. Skrandies, W. (1998). Evoked potential correlates of semantic meaning—A brain mapping study. Cognitive Brain Research, 6, 173–183. Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme. Yoshizaki, K. (2001). Effects of visual familiarity for words on interhemispheric cooperation for lexical processing. Cognitive Brain Research, 12, 409–414. Zaidel, E. (1976). Auditory vocabulary of the right hemisphere following brain bisection or hemidecortication. Cortex, 12, 191–211.