N400-like Semantic Incongruity Effect in 19-Month-Olds: Processing Known Words in Picture Contexts

Manuela Friedrich and Angela D. Friederici Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1465/1756938/0898929042304705.pdf by guest on 18 May 2021

Abstract & To understand mechanisms of early language acquisition, averaged across the group of 55 children revealed an N400- it is important to know whether the child’s acts in an like semantic incongruity effect in addition to an early phono- adult-like manner when processing words in meaningful logical–lexical effect. The results suggest that both contexts. The N400, a negative component in the event- lexical expectations facilitating early phonological processing related potential (ERP) of adults, is a sensitive index of and mechanisms of semantic priming facilitating integra- semantic processing reflecting neural mechanisms of semantic tion into semantic context are already present in 19-month- integration into context. In the present study, we investigated olds. The child’s specific comprehension abilities are whether the mechanisms indexed by the N400 are already reflected in strength, latency, and hemispheric differences working during early language acquisition. While 19-month- of the semantic incongruity effect. Spatio-temporal differ- olds were looking at sequentially presented pictures, they ences in that effect, thus, indicate changes in the organi- were acoustically presented with words that were either zation of brain activity correlated with the child’s behavioral congruous or incongruous to the picture content. The ERP development. &

INTRODUCTION Friederici & Hahne, 2001; Gonzalez-Garrido et al., The N400, a negative component in the event-related 1997; Holcomb, Coffey, & Neville, 1992; Friedman, potential (ERP) peaking around 400 msec after stimulus Sutton, Putman, Brown, & Erlenmeyer-Kimling, 1988), onset, is a sensitive index of semantic processing in up to now there is no study reporting N400-like context adults (e.g., Friederici, Pfeifer, & Hahne, 1993; Holcomb effects in children. However, there are two main reasons & Neville, 1991; Neville, 1985; Kutas & Hillyard, 1980). It why it is important to focus on the question whether an indicates that the meaningful context in which a stimu- N400 semantic incongruity effect is already present lus is presented influences the brain’s response to that during early language acquisition: stimulus. Stimuli that are semantically incongruous in First, nearly nothing is known about the neural mech- the current context release greater N400 amplitudes anisms of early word learning. Although it has already than a semantically congruous stimulus. This N400 been shown that negative components in the child’s semantic incongruity effect reflects the effort for stimu- ERP (, N350) are related to semantic aspects of lus integration into semantic context that is stronger for language processing, namely, to word comprehension unexpected than for expected stimuli. Thus, the neural (Mills, Coffey-Corina, & Neville, 1993, 1994), these stud- mechanisms of semantic integration indexed by the ies did not investigate word comprehension in the N400 can be facilitated by any kind of semantic priming semantic context. To learn about how children acquire prior to the stimulus presentation. The integration into lexical representations, it is, however, necessary to know semantic context held in working , however, how the child’s brain processes words in meaningful mainly depends on the organization of semantic knowl- contexts. This holds for both the first known words for edge in long-term memory (for a recent review, see which children have already established some kind of Kutas & Federmeier, 2000). lexical representation which, however, will probably be Although adult-like N400 effects have already been modified during the continuing course of language foundinschoolchildrenandeveninchildrenof acquisition, and for unknown words for which children preschool age (Hahne, Eckstein, & Friederici, under are going on to build up new lexical representations. submission; Coch, Maron, Wolf, & Holcomb, 2002; The critical question that we address in our study is whether adult-like mechanisms of semantic integration are already present at the beginning of the child’s language comprehension in ontogeny when they have Max Planck Institute for Human Cognitive and Brain Sciences learned their first words.

D 2004 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 16:8, pp. 1465–1477 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304705 by guest on 26 September 2021 Second, little is known about the kind of concepts ally assessed adults with identical stimuli in the same that the developing brain build up during early lan- paradigm to directly compare the spatio-temporal dis- guage acquisition. From behavioral studies, it is well tribution of the responses in children and adults. In known that children extend words to other exemplars order to investigate processing differences between (e.g., referring to a peach as ‘‘apple’’) resulting in a children who know most of the words presented during large number of overextensions (e.g., Gelman, Croft, the experimental session and those who know only a Fu, Clausner, & Gottfried, 1998). It is still under debate, few of the presented words, children were grouped post however, whether a child truly thinks that the word hoc according to their specific comprehension abilities ‘‘apple’’ refers to a peach, or even that an apple is the that were assessed by a comprehension rating scale. The same thing as a peach, or whether this overextension is definition of comprehension groups on the basis of Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1465/1756938/0898929042304705.pdf by guest on 18 May 2021 simply an error in the child’s productive use as the the experimental material itself should allow to control word ‘‘peach’’ has not yet been acquired. Although the effect of differences in the child’s a priori compre- behavioral measures can tell us something about the hension of the presented words. conceptual development of children and toddlers, the ERP technique allows for specific investigations of brain–behavior relations. As the N400 depends on the RESULTS organization of semantic knowledge in memory, it is a favored component for investigating the nature and Adults timing of use during language com- The ERP of adults (Figure 1) shows the typical N1–P2 prehension. If the neural mechanisms of semantic complex for auditory stimuli that is followed by a integration indexed by the N400 are already working negative–positive–negative wave pattern to both con- during early language acquisition, then the N400 will be gruous and incongruous words. Within the early tem- a powerful tool for investigating the development of poral range of the N1–P2 complex, there already occur concepts and the organization of semantic memory in small differences between word conditions at temporal children and toddlers. sites. Between 400 and 800 msec, a prominent negative In the present study, we used a picture–word-match- wave is present for incongruous words that at frontal ing paradigm with colored pictures of single objects and sites lasts up to 1200 msec. For congruous words, small slowly spoken basic level words to investigate whether negative responses can be observed only at frontal an N400-like response can be observed in 19-month-old sites between 400 and 500 msec and between 600 and children when they hear words that do not refer to 800 msec. At posterior sites congruous words show ongoing pictured objects. As the word stimuli used for three positive waves, an early one with a latency of ap- the children strongly differ in their duration from those proximately 300 msec that also occurs at anterior sites, typically used in N400 priming paradigms, we addition- a middle latency positivity between 500 and 600 msec,

Figure 1. ERPs of adults on slowly spoken words during picture–word matching. Solid lines for incongruous and dotted lines for congruous words.

1466 Journal of Cognitive Neuroscience Volume 16, Number 8 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304705 by guest on 26 September 2021 and a late one from 700 to 1600 msec (see also Figure 3 Table 1. Adult’s Condition Main Effects within Separate displaying the spatial distribution of the adult’s ERPs Condition (Congruous/Incongruous)  Region (Frontal/ within consecutive time windows of 200 msec duration). Central/Parietal) ANOVAs for Midline as well as for Left and Thus, differences between congruous and incongruous Right Hemispheric Sites words in the adult ERP start early and last a very long Time Left Midline Right time. The distribution of the negative difference wave Window Hemisphere, Sites, Hemisphere, between incongruous and congruous words seems to be (msec) F(1,19) F(1,19) F(1,19) relative stable over time with only slightly shifting to 300–400 9.070** 8.094* more anterior sites from earlier to later time windows (Figure 4). 400–500 4.533* 5.581* Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1465/1756938/0898929042304705.pdf by guest on 18 May 2021 A Condition  Region interaction [F(1,19) = 8.598, 500–600 10.164*** 26.234**** 19.662**** p < .01] for mean amplitudes within 100 to 250 msec revealed the existence of a regional condition effect 600–700 7.789* 11.361*** 11.419*** during very early processing stages. At temporal sites 700–800 12.777*** 9.650** in that time range, the response on congruous words 800–900 13.646*** 9.961** was significantly more negative than the response on incongruous words [F(1,19) = 5.708, p < .05]. 900–1000 12.798*** 32.876**** 29.367**** Main effects of condition within 300–400 msec 1000–1100 26.836**** 52.646**** 48.058**** [F(1,19) = 6.419, p < .05] and 500–1200 msec [F(1,19) = 1100–1200 8.901** 40.467**** 21.142**** 8.068–43.715, p < .0005–.05] with responses being more negative on incongruous than congruous words indi- 1200–1300 7.132* cated a long-lasting semantic incongruity effect that is 1300–1400 broadly distributed across the scalp. Condition  Hemi- sphere interaction revealed hemispheric differences 1400–1500 in the time windows of 700–1000 msec [F(1,19) = *p < .05; **p < .01; ***p < .005; ****p < .001. 5.091–6.891, p < .05] and 1200–1300 msec [F(1,19) = 4.617, p < .05]. There were no further interactions including condition. Separate two-way analyses for the left and right hemispheres showed that in the time long-lasting semantic incongruity effect is observed in range from 700 to 900 msec, an incongruity effect was the adult ERP that starts at about 300 msec and is most clearly present in the right hemisphere, but it did not prominent at centro-parietal midline sites as well as it is reach significance in the left hemisphere (Table 1). By stronger and temporally more extended in the right separate two-way analyses for congruous and incon- hemisphere than in the left one. This pattern of the gruous words, it could be specified that there were no observed incongruity effect matches the spatial distribu- significant hemispheric differences in the response on tion of the typical N400 effect in semantic priming congruous words while the response on incongruous paradigms that has a centro-parietal maximum and is words was more negative in the right hemisphere than slightly right lateralized. Nevertheless, anterior regions, in the left one within the time windows from 700 to to a certain extent, are also involved in the incongruity 1000 msec [F(1,19) = 6.013–8.816, p < .05] and from effect. 1100 to 1300 msec [F(1,19) = 4.786–4.916, p < .05]. For midline sites, a main effect of condition was present in 19-Month-Old Children each time window from 300 to 1300 msec (Table 1). Condition  Region interactions observed within 300 to In the ERP of 19-month-old children (Figure 2), there 400 msec [F(1,19) = 4.712, p < .05] and 700 to 800 msec occurs a positive component at a latency of 120 msec [F(1,19) = 4.416, p < .05] were caused by the fact that and a negativity at about 190 msec instead of an adult- the early incongruity effect did not reach significance at like N1–P2 complex. This complex is followed by a small FZ. While for incongruous words the response in the positive deflection at approximately 230 msec and a interval of 300 to 400 msec was more negative at CZ and second negativity at about 320 msec. Within the time PZ than at FZ [main effect of region: F(2,38) = 8.849, range of these early components, congruous words p < .001], this effect could not be observed for congru- release more negative responses at lateral frontal sites. ous words. At posterior sites, there occurs a broad negative wave, To summarize, for slowly spoken word stimuli in a already prominent before 400 msec with two local picture–word-matching paradigm appropriate for chil- maximums at about 550 and 800 msec. This negative dren, a condition effect restricted to temporal sites response has a greater amplitude and lasts longer indicates that in adults, word processing is already for incongruous than for congruous words. At anterior affected by picture contexts during very early processing sites, congruous words elicit a series of three positive stages. Following that early effect, a broadly distributed waves approximately from 400 to 550 msec, from 600 to

Friedrich and Friederici 1467 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304705 by guest on 26 September 2021 Figure 2. ERPs of 19-month-old children on slowly spoken words during picture–word matching. Solid lines for incongruous and dotted lines for congruous words. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1465/1756938/0898929042304705.pdf by guest on 18 May 2021

1000 msec, and from 1100 to 1500 msec. Whereas the in the last time range, incongruous words rather show a first positivity occurs for incongruous words to the same negative response (see also Figure 3 displaying the extent as for congruous words, the second one is much spatial distribution of the child’s ERPs within consecu- weaker on incongruous than on congruous words, and tive time windows of 200 msec duration). Thus, similar

Figure 3. Spatial distribution of adult’s and child’s ERPs on congruous and incongruous words within consecutive time windows of 200 msec duration.

1468 Journal of Cognitive Neuroscience Volume 16, Number 8 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304705 by guest on 26 September 2021 to adults, broadly distributed differences between con- until 1400 msec. Although there seems to be slightly gruous and incongruous words can be observed during different spatio-temporal distributions at midline sites, long time intervals in the child’s ERP. The negative this could not be statistically verified by Condition  incongruity effect in the grand average seems to mainly Region interactions. be focused on two areas, a left parietal and a frontal To summarize, children at an age of 19 months show a one, which is suggested by the spatial distribution of the very early context effect in their ERPs that is followed child’s difference wave between incongruous and con- by a broadly distributed negative incongruity effect. At gruous words (Figure 4). Inspection of the individual midline sites, the child’s semantic incongruity effect averages revealed that about 80% of the children display reaches significance 400 msec later and lasts 100 msec a negative difference between incongruent and congru- longer than that in adults. The missing of topological Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1465/1756938/0898929042304705.pdf by guest on 18 May 2021 ent words in at least one region. differences at midline sites indicates that in children, the Within the early time window of 150 to 400 msec, a frontal region is involved in processing semantic incon- Condition  Region interaction clearly reached signifi- gruity at least to the same extent as the centro-parietal cance [F(1,54) = 9.509, p < .005], suggesting that a very region. Although for children, there were no statistically early context effect occurred even in 19-month-old significant hemispheric differences, the left hemisphere children. Similar to adults, in that time range, congruous appears to contribute stronger to the incongruity effect words elicited more negative responses than incongru- than in adults. Thus, the spatio-temporal distribution of ous words. This condition effect, however, occurred at the semantic incongruity effect observed in the group of F7 and F8 [F(1,54) = 4.22, p < .05], that is, anterior to 55 children differs from that of adults. that in adults. Main effects of condition with incongruous words Comprehension Groups being more negative than congruous words occurred from 800 to 900 msec [F(1,54) = 6.034, p < .05], from According to the parent’s comprehension rating, child’s 900 to 1000 msec [F(1,54) = 4.240, p < .05] as well mean proportion of comprehended words was 81.26%. as from 1100 to 1400 msec [F(1,54) = 4.715–6.899, The median for the number of comprehended words p < .05]. There were no further interactions including in parental ratings was 37. Within the high comprehen- condition. sion group of 13 boys and 14 girls, the median was As visual inspection suggested that the incongruity 42 with at least 38 comprehended words and maximal 44 effect was larger in the left than in the right hemi- comprehended words. The low comprehension group sphere, we performed separate two-way analyses for included 17 boys and 11 girls who had a median of 33 both hemispheres. While in the right hemisphere with a minimum of 6 and a maximum of 37 compre- the incongruity effect reached significance only from hended words. 1200 to 1400 msec, in the left hemisphere it was pre- The early fronto-temporal context effect did not sent within 800 to 1000 msec and 1100 to 1400 msec change as a function of comprehension group. In con- (Table 2). At midline sites the incongruity effect al- trast, for the later negative incongruity effect group ready started at 700 msec and was continuously present differences could be observed. Condition  Hemisphere

Figure 4. Spatial distribution of adult’s and child’s difference wave between incongruous and congruous words within consecutive time windows of 200 msec duration.

Friedrich and Friederici 1469 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304705 by guest on 26 September 2021 Table 2. Child’s Condition Main Effects within Separate 600 msec [F(1,53) = 7.763–11.060, p < .01], from 600 Condition (Congruous/Incongruous)  Region (Frontal/Cen- to 700 msec [F(1,53) = 4.875, p < .05], and from 800 tral/Parietal) ANOVAs for Midline as well as for Left and Right to 1000 msec [F(1,53) = 4.794–5.934, p < .05] (see Hemispheric Sites Figure 6 displaying the spatial distribution of the ERPs Time Left Midline Right on incongruous words for the two comprehension Window Hemisphere, Sites, Hemisphere, groups). (msec) F(1,54) F(1,54) F(1,54) To summarize, children with lower comprehension abilities show only a small semantic incongruity effect in 300–400 the left hemisphere that occurs much later than in 400–500 adults. In contrast, children with high comprehension Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1465/1756938/0898929042304705.pdf by guest on 18 May 2021 500–600 abilities produce a large semantic incongruity effect starting in the same time window as in adults. Although 600–700 children with high comprehension abilities, like adults, 700–800 5.960* produce a stronger semantic incongruity effect in the right hemisphere, the spatio-temporal distribution of 800–900 8.046** 7.558** their effect does not exactly match that of adults as 900–1000 5.248* 5.191* frontal areas are stronger involved in children than in 1000–1100 4.057* adults. 1100–1200 4.873* 5.808* 1200–1300 6.197* 7.039* 5.455* DISCUSSION 1300–1400 5.181* 9.460*** 6.903* In the present study, we investigated the ERP response of 1400–1500 adults and 19-month-old children on slowly spoken basic level words during picture–word matching. While *p < .05; **p < .01; ***p < .005. a typical auditory N1–P2 complex was evoked in the ERP of adults, children displayed an early positive–negative waveform at approximately the latency of the adult N1– P2 complex. This early waveform represents an auditory-  Group interactions indicated hemispheric differences evoked response that is characteristic in children and in the incongruity effect between low and high com- prehension groups in the temporal ranges from 300 to 600 msec [F(1,54) = 6.159–10.012, p < .005–.05] and from 800 to 1200 msec [F(1,54) = 4.336–6.684, p < .05] Table 3. Condition Effects of the High Comprehension Group that were specified by separate analyses of left and right within Separate Condition (Congruous/Incongruous)  Region (Frontal/Central/Parietal) ANOVAs for Midline as well as for Left hemispheres within each comprehension group. In the and Right Hemispheric Sites high comprehension group, an early negative incon- gruity effect was already present between 300 and Time Left Right 400 msec in the right hemisphere but not in the left Window Hemisphere, Midline, Hemisphere, one. The high comprehension group displayed further (msec) F(1,26) F(1,26) F(1,26) condition effects in the right hemisphere within 600 300–400 4.558* and 1000 msec as well as within 1100 and 1200 msec (Table 3). For the low comprehension group, no condi- 400–500 tion effect was found in the right hemisphere. In the 500–600 left hemisphere, a significant incongruity effect was 600–700 5.107* 5.309* present from 700 to 900 msec for the high compre- hension group (Table 3) and from 1200 to 1300 msec 700–800 4.624* 6.953* 5.359* for the low comprehension group [F(1,27) = 4.271, 800–900 5.130* 6.842* 7.436* p < .05] (Figure 5). 900–1000 5.807* 5.635* While the response on congruous words seems to be generally more positive in the high comprehension 1000–1100 group than in the low comprehension group which, 1100–1200 4.896* 6.212* however, could not be statistically verified, hemispheric differences in the incongruity effect between the groups 1200–1300 were caused by incongruous rather than by congruous 1300–1400 words. This was indicated by Hemisphere Group  1400–1500 interactions for incongruous words, which in separate analyses of the two conditions, occurred from 300 to *p < .05.

1470 Journal of Cognitive Neuroscience Volume 16, Number 8 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304705 by guest on 26 September 2021 Figure 5. ERPs of low and high comprehension groups on slowly spoken words during picture–word matching. Solid lines for incongruous and dotted lines for congruous words. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1465/1756938/0898929042304705.pdf by guest on 18 May 2021

young children (e.g., Morr, Shafer, Kreuzer, & Kurtzberg, tive components within a similar time range had been 2002; Kushnerenko et al., 2001; Mills et al, 1993, 1994; shown to differentiate the processing of known words Kurtzberg, Stone, & Vaughan, 1986). from that of unknown and backward presented words For both adults and children, clear differences were in 20-month-old children (Mills et al., 1993). Under the found between the ERP to words that match the cur- interpretations that known words elicited larger early rent picture and words that do not. During early negativities than unknown stimuli, our finding might time intervals (for adults: 100–250 msec; for children: be viewed to show that congruous words are better 150–400 msec), congruous words elicited more negative known than incongruous words. As, however, the same responses than incongruous words. Interestingly, nega- words were used in congruous and incongruous word

Figure 6. Spatial distribution of the ERPs on incongruous words for low and high comprehension groups within consecutive time windows of 200 msec duration.

Friedrich and Friederici 1471 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304705 by guest on 26 September 2021 conditions, there are no differences concerning their children and its presence in 19-month-old children primary comprehension. It is only by the picture context might indicate that the mechanisms indexed by the that congruous words may be perceived as ‘‘better N400 develops between an age of 14 and 19 months. known’’ than incongruous words. Thus, we interpret There are, however, several differences in the method- this early context effect as reflecting a top-down priming ology between our study and that of Molfese and his that facilitates mechanisms of early phonological–lexical colleagues such that it might also be possible that an processing of content words. This interpretation is also N400-like response develops even earlier. Thus, further in line with results of semantic and word fragment research is required to specify the age at which the N400 priming in adults (Friedrich, Kotz, Friederici, & Gunter, occurs for the first time. in press; Nobre & McCarthy, 1994). In our study, the spatio-temporal distribution of the Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1465/1756938/0898929042304705.pdf by guest on 18 May 2021 Whereas in the study of Mills and her colleagues the N400 incongruity effect differed between 19-month-old difference between known and unknown words mainly children and adults. In adults, the N400 had a centro- occurred over temporal and parietal regions of the left parietal maximum with stronger responses in the right hemisphere, the difference between known and back- than in the left hemisphere, and with only a small effect ward words included frontal, temporal, and parietal sites at frontal sites. In children, frontal areas were strongly of both hemispheres. In our study, children showed an involved in processing semantic incongruity. Moreover, early context effect at fronto-lateral sites while the it appears that there are two distinct incongruity effects, adult’s effect in the same paradigm was restricted to a left lateralized parietal and an anterior one. In adults, temporal sites. The spatial differences between the such anterior N400-like negativities had been observed child’s effects in both studies may result from the in response to semantically incongruous pictures (West different paradigms used. As we presented words in & Holcomb, 2002; Federmeier & Kutas, 2001; McPher- picture contexts that initially were equally well known son & Holcomb, 1999; Ganis, Kutas & Sereno, 1996; by the children, the observed effect in our study reflects Holcomb & McPherson, 1994; Barrett & Rugg, 1990), a difference between known unprimed and known and in response to concrete nouns, that is, words re- primed words. In contrast to the difference between ferring to pictureable objects (Friedrich, van der Meer, & known and unknown words, this priming effect oc- Ullsperger, under submission; West & Holcomb, 2000; curred bilaterally similar to the difference between Holcomb, Kounios, Anderson, & West, 1999; Kounios & known and backward words. The more anterior distri- Holcomb, 1994). These anterior negativities in the tem- bution in our children compared with those from the poral range of the N400 are assumed to reflect image- study of Mills and her colleagues might result from a specific semantic processing that is functionally similar temporal overlap of that early effect with the onset of to the processing of amodal semantic information in- the centro-parietal negative incongruity effect observed dexed by the centro-parietal N400, but possibly sup- in our study. In adults, however, the early priming effect ported by different brain regions (West & Holcomb, occurred still earlier than in children such that it did not 2002). overlap with the semantic incongruity effect. In the present study, we used a picture–word-match- During its later time course, the child’s difference ing paradigm with words naming basic level concepts wave between incongruous and congruous words had that are commonly seen as most inclusive concepts for a clear negative polarity. As the same physical stimuli which a concrete image can be formed (Rosch, Mervis, had been used in congruous and incongruous word Gray, Johnson, & Boyes-Braem, 1976). At the time when conditions, these differences were exclusively caused a word was presented the picture was already present by the semantic context provided by the picture. Thus, on the screen. Thus, this paradigm induces some image- for the first time, we observed an N400-like semantic based processing that is reflected in the presence of an incongruity effect in children below the age of 2 years. anterior part of the N400. As, however, children and Up to now, there exists only one other child study adults were presented with the same stimulus material, that explored the child’s processing of word-like stimuli topological differences in their incongruity effects must in meaningful contexts (Molfese, Morse, & Peters, 1990). be caused by maturational changes. The strong involve- In this study with 14-month-old children, the ERP re- ment of anterior regions in the child’s incongruity effect sponse on two different pseudowords (‘‘gibu’’ and might therefore reflect an enhanced image-specific se- ‘‘bidu’’) that were used by parents to name novel objects mantic processing of incongruous basic level words differed depending on whether the pseudoword which occurs in children during early language acquisi- matched the trained name of a presented real object tion but not in adults. Alternatively, developmental or not. The authors reported two different responses, a differences in N400 topography might also be caused very early negativity at a latency of about 60 msec and a by the presence of the frontally distributed Nc, a com- positivity at about 560 msec, that discriminated the ponent that reflects increased attention or processing mismatching from the matching trials. There was, how- load in children (e.g., Courchesne, 1990). If incongruous ever, no evidence for an N400-like incongruity effect. words capture the child’s attention more than congru- The absence of an adult-like N400 in 14-month-old ous words or if they require enhanced processing load

1472 Journal of Cognitive Neuroscience Volume 16, Number 8 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304705 by guest on 26 September 2021 then the frontal Nc may possibly overlap with the comprehension group displayed a left hemispheric to centro-parietal N400. bilateral distribution of the negativity on incongruous In children, not only incongruous but also congruous words, causing an incongruity effect over the left but not words elicited a negative response. An N400-like nega- over the right hemisphere. In the high comprehension tivity on congruous words realized as best sentence group, in contrast, incongruous words released a right completions had also been observed in 5- to 14-year- hemispheric distributed response that results in an in- old children. The change of this negativity’s amplitude congruity effect that is stronger over the right than the during development is assumed to reflect an overall left hemisphere. Similar differences in the hemispheric decline in responsiveness to context with age (Holcomb specialization were already reported for 20-month-old et al., 1992). In this study with older children, the children for words presented out of context (Mills et al., Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1465/1756938/0898929042304705.pdf by guest on 18 May 2021 negativity on best completions was greatest at anterior 1993). Within this study, a frontally distributed negativity sites. In our study with children, however, the negativity between 600 and 900 msec occurred in response to on congruous words occurred at posterior sites. As there known and unknown words as well as to word-like is a tendency for this negativity to be more prominent in stimuli (backward words). Although neither amplitude children with low than with high comprehension abili- nor topological distribution of this N600–N900 wave was ties, it may reflect the child’s effort in accessing the affected by the different stimulus types, differences meaning of words that are congruous to the picture could be observed when children were grouped accord- context. Such an effort would be expected, because at ing to their speech abilities. Both comprehended and that age the children are not always able to easily access unknown words elicited larger negative responses in the full meaning of each word presented during the children with low than high productive vocabulary. experimental session. Moreover, for the low production group, the N600– An N400-like incongruity effect, however, was ob- N900 displayed a bilateral distribution, while for the served even though according to the parent’s rating, high production group, it was largest over the right on average nearly 20% of the words were not understood hemisphere. In the study of Mills and her colleagues, by the children. The fact that the negative incongruity the child’s speech abilities were assessed by a test that effect was stronger in children who comprehended the was independent of the material presented during the meaning of most of the words tested than those experimental session. The similar hemispheric group who comprehended only a few words tested supports effects in both studies suggest that the spatio-temporal the interpretation that the effect indeed reflects different differences between high and low comprehension group semantic processing of congruous and incongruous in our study may not only be caused by the compre- words, and thus, represents a child N400. hension differences of those words presented during the Interestingly, there was no difference between the experimental session, but, to some extent, they might comprehension groups with regard to their early fronto- also reflect processing differences as a function of the temporal context effect that indicates phonological– child’s general language abilities. lexical facilitation during the processing of congruous In our study, children’s specific language abilities also words. This finding implies that children of both com- affected the time course of the incongruity effect. While prehension groups were already able to create appropri- children with low comprehension abilities displayed ate lexical expectations from the picture content. That only a very late N400-like effect, in children of the high is, the semantic content of the pictures primed the comprehension group, the incongruity effect started associated phonological–lexical representations even in as early as in adults. At first sight, this seems surprising, children that, according to the parental rating, compre- as for auditory sentence comprehension decrease in hended some, but not all, of the presented words. In N400 latency had been reported for children from 5 to that group, contrary, the phonological representations 13 years (Hahne et al., under submission; Holcomb of the words did not always prime specific semantic et al., 1992). However, in our study, we used a different representations that are sufficient to facilitate integration experimental paradigm, and moreover, instead of peak into semantic context. Thus, although the parents rated amplitude and latency as measured by Holcomb and the specific comprehension abilities in children of the colleagues, we analyzed averaged amplitudes within two comprehension groups to be different, children of different time windows such that our results cannot both groups appear to possess similar mechanisms directly be compared to these developmental studies. allowing lexical expectations which in turn suggests There are, however, two reasons for why it is possible the existence of some lexical–semantic knowledge. The that the child’s N400-like response shows the same time integration of this knowledge into the semantic context course as the adult N400. First, the stimulus material is the specific ability that differed between the groups. used in the present study was especially developed to The comparison of children with low and high com- be suitable for children below the age of 2 years. That prehension abilities further revealed clear differences in is, pictures were simple colored illustrations that are their topological organization of brain activity during the clearly identifiable, and words were slowly spoken semantic processing of incongruous words. The low names of those basic level concepts that are known to

Friedrich and Friederici 1473 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304705 by guest on 26 September 2021 be first acquired by children. The semantic integration of and hemispheric differences of the N400 incongruity a word into the picture context, furthermore, did not effect. These morphological differences are taken to require any temporal maintaining of information in indicate changes in the organization of brain activity memory as the words occurred at the time when a correlated with the child’s behavioral development. picture was still present on the screen. And, second, as slow presentation rates delay the N400 response in adults (Holcomb & Neville, 1991), it is not really sur- METHODS prising that children who comprehend nearly all of the presented words respond on semantic incongruity as Stimuli fast as adults. Stimuli taken as items in the picture–word-matching Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1465/1756938/0898929042304705.pdf by guest on 18 May 2021 Interestingly, our results show that children at an age paradigm were selected in such a way that 19-month- of 19 months are able to integrate the meaning of a old children are able to comprehend most of them. All word into its context definitely before the whole acous- of the 44 words used were items of the ELFRA 1 (Grimm tic information has been presented. In the high com- & Doil, 2000), the German analog of the MacCarthur prehension group, the incongruity effect started at Communicative Development Inventories (Fensen et al., about 300 msec while mean word length exceeded a 1993), with a mean item difficulty (comprehension duration of 1000 msec. This means that 19-month-old at an age of 18 months) of 78.04%. Words were basic children, similar to adults (e.g., Zwitserlood, 1989), level names with mean word length of 1083 msec, spo- access lexical information even when the auditory input ken in a child-directed manner, that is, very slowly. is only partly presented, that is, they are already able to During the experimental session, they were presented extract semantic information from the beginnings of a via a loudspeaker with an intensity of approximately word. This result is in line with a behavioral picture– 65 dBSPL. As congruous and incongruous words were word study in which 18-month-old children were shown exactly the same, congruous and incongruous condi- to be capable of using word-initial phonetic information tions only differed in the picture context in which they to understand fluent speech (Fernald, Swingley, & Pinto, were presented. 2001). Moreover, the finding that children with faster reaction times had a larger productive vocabulary than Procedure children with slower response latencies goes with our ERP result revealing that children with low word com- During the EEG recordings, participants were seated prehension displayed the N400 incongruity effect much in front of a TFT-LCD computer screen (distance for later than children with high word comprehension. As children about 1 m, for adults about 1.5 m) in a dimly perceptual and semantic difficulties are reflected in the lit, electrically shielded and sound-insulated experimen- N400 latency (i.e., Holcomb & Neville, 1991; Holcomb, tal room. The total experimental session lasted about 1993), this delay in the low comprehension group 12 min. At each trial, a colored picture of a single object appears to be caused by difficulties in their perceptual appeared for 4000 msec on the screen. After an interval and semantic processing. of 900 msec from picture onset, an indefinite article was acoustically presented which 1000 msec later, while the picture was still seen on the screen, was followed by a Conclusion word or a word-like stimulus. Words were either correct Children at an age of 19 months show a negative com- basic level names of the pictured objects or basic level ponent in their ERP that is prominent when they hear names of other objects (i.e., either congruous or incon- words that do not refer to ongoing pictured objects. gruous to the picture meaning). Congruous and incon- According to its spatial, temporal, and functional sim- gruous words presented to the same picture always ilarity with the adult N400, this component is in- differed in their first phonemes. Additionally, pseudo- terpreted as a child N400. The strong involvement of words and nonwords were presented. Here we report anterior regions in the child’s semantic incongruity only data from word stimuli. Each word was presented effect seems to reflect the important part of image- two times, once in congruous and once in incongruous specific semantic processing at that age. The occurrence picture contexts. of an additional phonological–lexical priming effect pre- ceding the semantic incongruity effect suggests that Participants lexical expectations are created from meaningful pic- tures even by children at an age of 19 months. The The present study is part of the German Language presence of a child N400 at this age implies that adult- Development Study (GLaD; www.glad-study.de). Fami- like mechanisms of integrating word meaning into se- lies participate in the study according to institutional mantic context already work when children have learned signed informed consent procedures. For participation their first words. The child’s abilities in comprehending in the study, full-term children were chosen by pedia- the presented words are reflected in strength, latency, tricians on the basis of a normal course of pregnancy

1474 Journal of Cognitive Neuroscience Volume 16, Number 8 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304705 by guest on 26 September 2021 and a normal birth. They were healthy and without cap (Easy Cap, Falk Minow). During the recordings, the neurological or developmental problems. Only children ERP electrodes were referenced to CZ. Electrooculo- with monolingual experience with German participate in grams (EOG) were bipolar recorded from supraorbital the GLaD study. For attendance in the ERP study, and infraorbital electrodes on the right eye as well as parents received a compensation of A 30. from electrodes located lateral to the left and to the A total of 20 adults (mean age 23.7 years, 10 men, right eye. Electrode impedances were below 5 k for 10 women) and 80 children were assessed. The child adults and in children mostly below 10 k , at least below EEG recordings were taken when they were 19 months 20 k . The EEG was amplified with PORTI-32/MREFA old (±7 days). During the EEG recordings, the children (Twente Medical Systems, with input impedance of were sitting on the mother’s or father’s lap. Their 1012 and analog first-order low-pass filter of 5 kHz), Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1465/1756938/0898929042304705.pdf by guest on 18 May 2021 behavior was continuously observed via a video-monitor digitized on-line at a rate of 500 Hz (AD converter with to determine whether the children were looking at the 22 bit, digital filter from DC to 125 Hz), and stored on pictures. In 13 children the recordings were broken off hard disk. Further analyses were processed off-line. when they were crying or did not stop moving exces- The EEG was algebraically re-referenced to the aver- sively. Data from 12 children were excluded from the age of left and right mastoids (A1, A2). A zero-phase analyses as these children either produced too many digital band-pass filter ranging from 0.3 to 20 Hz (À3dB artifacts (fewer than 20 trials per condition) or, during cutoff frequencies of 0.43 and 19.87 Hz) was applied to long periods, they were not looking at the pictures on increase the signal-to-noise ratio by removing slow drifts the monitor. In the analyses presented here, we in- and muscle artifacts. Trials exceeding a standard devia- cluded only those children who were looking on the tion of 40 AV for adults, and 100 AV for children within pictures in at least 70% of the trials. A total of 55 children a sliding window of 200 msec were rejected automat- (30 men, 25 women) entered the final analyses. On aver- ically. We used this rejection method instead of a age, these children were looking to the monitor during method based on eye electrodes only because in chil- about 85% of the whole session. Due to technical dren body movements such as leaning forward and restriction, we also include trials of the remaining 15% pointing to the pictures, shaking one’s head, or turning in the average. As, however, the nonlooking trials were around to their parents produced much stronger arti- often accompanied with motor movement, most of facts than blinks and horizontal eye movements. Epochs these trials were excluded as artifacts. The mean portion of 1600 msec from stimuli onset were averaged accord- of trials seen by the children did not differ between the ing to a 200-msec prestimulus baseline. At least 20 comprehension groups. artifact-free trials were required for an individual average to be included in further analyses. The mean number of accepted trials was 32. This number did not differ be- Comprehension Rating Scale tween the conditions. After the child’s experimental session, parents were ask to rate for each of the 44 words that were presented Data Analyses during the experiment whether or not their child al- ready comprehends the meaning of the word. The For investigating the early lexical incongruity effect, in results of this rating scale were used to group the adults mean amplitudes within 100 to 250 msec were children into two groups with the median of 37 com- calculated at F7, F8, T3, and T4. Due to different prehended words as cut off criteria, hereafter labelled latencies in the child ERPs, a later time interval of low and high comprehension group. This was done in 150 to 400 msec was chosen for the 19-month-old chil- order to evaluate whether possible ERP effects are dren. Three-way repeated-measures analyses of variance related to the children’s specific abilities in compre- (ANOVAs) with Condition (congruous/incongruous), Re- hending the words presented during the experimental gion (frontal/temporal), and Hemisphere (left/right) session. Thus, this grouping did not necessarily assess were conducted to evaluate the early amplitude differ- differences between children with different comprehen- ences between congruous and incongruous words. sion abilities in general, but rather differences in the The N400-like semantic incongruity effect was ana- responses to comprehended and unknown words, lyzed in the temporal range from 200 to 1500 msec. which might occur even within one subject. For each condition at each electrode site, mean ampli- tudes were calculated within consecutive time windows of 100 msec duration. Regions of interests were analyzed ERP Recording and Averaging with each region combining two electrode sites. The left The EEG were continuously recorded from silver–silver frontal region included F3 and FC3, the right frontal chloride electrodes at sites F7, F3, FZ, F4, F8, FC3, FC4, region F4 and FC4, the left central region C3 and T3, the T3, C3, C4, T4, CP5, CP6, T5, P3, PZ, P4, T6, O1, O2, A1, right central region C4 and T4, the left parietal region and A2 (according to the 10–20 International System of P3 and CP5, and the right parietal region P4 and CP6. Electrode Placement) attached to an elastic electrode To assess incongruity effects as well as topological as-

Friedrich and Friederici 1475 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304705 by guest on 26 September 2021 pects of these effects, three-way ANOVAs with Condition perceptual predictability on picture processing. Journal of (congruous/ incongruous), Region (frontal/ central/ pa- Experimental Psychology: Learning, Memory, and Cognition, 27, 202–224. rietal), and Hemisphere (left/right) as within-subject Fensen, L., Dale, P. S., Reznick, J. S., Bates, D., Hartung, J. P., factors were carried out. Significant interactions were Pethick, S., & Reilly, J. S. (1993). MacCarthur further analyzed by two-way and one-way ANOVAs. communicative development inventories. San Diego, CA: For midline sites, two-way ANOVAs with Condition Singular Publishing. (congruous/incongruous) and Region (FZ/CZ/PZ) were Fernald, A., Swingley, D., & Pinto, J. P. (2001). When half a word is enough: Infants can recognize spoken words using performed. partial phonetic information. Child Development, 72, The comprehension groups were formed according to 1003–1015. the results of the parental ratings in the comprehension Friederici, A. D., & Hahne, A. (2001). Developmental patterns Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1465/1756938/0898929042304705.pdf by guest on 18 May 2021 rating scale. All children with rated comprehension abil- of brain activity for semantic and syntactic processes. In ities below the median formed the low comprehension B. Ho¨hle & J. Weissenborn (Eds.), Approaches to bootstrapping in early language development group, children with rated comprehension abilities above (pp. 231–246), Amsterdam: John Benjamins. the median were taken as high comprehension group. Friederici, A. D., Pfeifer, E., & Hahne, A. (1993). Event-related ANOVAs with Condition (congruous/incongruous), Re- brain potentials during natural speech processing: Effects of gion (frontal/ central/ parietal), and Hemisphere (left/ semantic, morphological and syntactic violations. Cognitive right) as within-subject factors, and Group as between- Brain Research, 1, 183–192. Friedman, D., Sutton, S., Putnam, L., Brown, & subject factor were calculated to assess group differences Erlenmeyer-Kimling, L. (1988). ERP components in picture within the morphology of the condition effect. matching in children and adults. Psychophysiology, 25, In all ANOVAs the Greenhouse–Geisser correction 570–590. (Greenhouse & Geisser, 1959) was applied, whenever Friedrich, C. K., Kotz, S. A., Friederici, A. D., & Gunther, T. C. there was more than one degree of freedom. Here, we (in press). ERPs reflect lexical identification in word fragment priming. Journal of Cognitive Neuroscience. report uncorrected degrees of freedom, and adjusted Friedrich, M., van der Meer, E., & Ullsperger, P. (under p values. submission). Functional dissociation between early and late component in the N400 during picture–word matching. Ganis, G., Kutas, M., & Sereno, M. (1996). The search for Acknowledgments ‘‘Common Sense’’: An electrophysiological study of the We thank Christina Ru¨gen and Jo¨rdis Haselow for their comprehension of words and pictures in . Journal of empathy in treating our subjects and their commitment in Cognitive Neuroscience, 8, 89–106. recording the ERP data. The data characterizing the devel- Gelman, S. A., Croft, W., Fu, P., Clausner, T., & Gottfried, G. opmental state of our subjects were kindly provided by Volker (1998). Why is a pomegranate an apple? The role of shape, Hesse, head of the pediatric clinic of the Krankenhaus taxonomical relatedness, and prior lexical knowledge in Lichtenberg, teaching hospital of the Charite´, Berlin. He and children’s overextensions of apple and dog. Journal of Child his team took care of the somatic and neurological data of the Language, 25, 267–291. children and he provided resources and manpower for Gonzalez-Garrido, A. A., Oropeza de Alba, J. L., Riestra recruiting subjects. This study was supported by the Deutsche Castaneda, R., Riestra Castaneda, J. M., Perez Avalos, M. Forschungsgemeinschaft (DFG, German Research Foundation) C., & Valdes Sosa, M. (1997). Event related brain (FR-519/18-1). potentials to semantically incongruent words in children of different ages. Archives of Medical Research, 28, Reprint requests should be sent to Manuela Friedrich, Max 109–113. Planck Institute for Human Cognitive and Brain Sciences, Greenhouse, S. W., & Geisser, S. (1959). On methods in the P.O. 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