Understanding the myriad of operations underlying language comprehension in the brain is an ongoing challenge in the field. Neuronal networks supporting these operations must dynamically assemble locally and flexibly communicate across long distances. But how does the brain do this? A growing number of studies on the oscillatory dynamics during language processing are revealing new insights into these mechanisms (for a review, see Bastiaansen and Hagoort, 2006). Oscillatory synchronization is thought to reflect the transient formation of functional brain networks (Varela et al., 2001; Fries, 2005), and this synchronization can be measured through EEG or MEG spectral analysis. Power analysis is thought to reflect the recruitment of local neuronal networks while coherence analysis reflects dynamic linking between brain areas involved in a global network. Additionally, analyzing oscillatory dynamics may reveal a rich set of information that is not currently seen during event-related potential (ERP) analysis because the ERP tends to average out non-phase-locked signals. Thus the study of oscillatory dynamics is a promising method to complement current ERP analysis and examine functional networks for language processing.

The network dynamics of lexical-semantic processing are still not fully understood. Previous studies have indicated that theta oscillations (4–7 Hz) are involved in these networks for lexical-semantic retrieval. Bastiaansen et al. (2005) observed greater theta power increases between 300 and 500 ms when subjects read open class (OC) words compared to closed class (CC) words in a short story context. Since OC words carry more semantic information than CC words, they are thought to probe lexical-semantic retrieval processing more deeply than CC words. In addition, these authors observed greater alpha (8–12 Hz) power decreases between 300 and 500 ms at right occipitotemporal electrodes for OC than CC words. Thus alpha power decreases may also be related to semantic retrieval. A study comparing nouns with different semantic features (primarily visual vs. auditory) also found differences in theta power increases between 100 and 400 ms (Bastiaansen et al., 2008). The theta effect was larger for the “visual” nouns at occipital electrodes while it was larger at temporal electrodes for “auditory” nouns suggesting that theta scalp topography reflects the sensory features of the words. Both studies point to a role for theta oscillations in the retrieval of lexical-semantic information, but the robustness of this effect has yet to be fully established.

In the present study, we focus on the role of oscillatory dynamics in retrieving OC vs. CC words. Specifically, we want to investigate the robustness of the previously established theta and alpha effects in different contexts and in a different population. Our motivation stems from how the factors of context and age affect the well-studied N400 ERP component. The N400 is a negative-going potential between 300 and 500 ms that reflects lexical-semantic processing. Evidence shows that the N400 is modulated by both the class (e.g., Van Petten and Kutas, 1991; Nobre and McCarthy, 1994; King and Kutas, 1995; Münte et al., 2001) and context of words (e.g., Kutas and Hillyard, 1980, 1984). An interaction between word class and context has also been reflected in the N400 (Van Petten and Kutas, 1991). Thus we have chosen to experimentally manipulate both word class (OC, CC) and context (sentence, scrambled sentence) in this study to further investigate any interaction between the two factors on the oscillatory dynamics during word reading. Aging also affects the amplitude and latency of the N400 (Harbin et al., 1984; Gunter et al., 1992; Kutas and Iragui, 1998), and could potentially modulate oscillatory responses. So far, the oscillatory dynamics of lexical-semantic processing have not been investigated in an older population (Bastiaansen et al., 2005 tested younger participants, aged 21–28) though the changes in the N400 suggest that there may be changes in the underlying semantic processing mechanisms with age. Hence we have chosen to test in an older population. An additional aim is to examine gamma band (>30 Hz) dynamics. This will extend the previous study on OC and CC words (Bastiaansen et al., 2005) which did not examine gamma oscillations though prior research has suggested that it is involved in lexical-semantic processing (Pulvermüller et al., 1999; Mainy et al., 2008).

To summarize, we will be testing for word class and context effects in older subjects as well as for any interaction between these factors. We predict that modulation of theta and alpha power will reflect greater lexical-semantic processing for OC words than CC words. Additionally, we expect that an interaction between class and context will reflect how word-level and sentence-level processing interact.

The evoked analysis only revealed activity centered at 150 ms in the alpha-band. Additionally, we did not find any significant effects in the evoked responses for either the OC–CC comparison (Figure 2A) or the sentence–scrambled sentence (S–SS) comparison (Figure 2B). The significant effects presented below thus reflect induced activity.

In order to examine the role of oscillatory dynamics during lexical-semantic processing in an older population, we studied changes in power as subjects read OC and CC words in different contexts. Our results indicate that alpha (8–12 Hz) oscillations are differentially involved in reading words of different class, while both alpha and low beta (13–18 Hz) are implicated in reading words in different contexts. To follow-up on the previous study of OC and CC words (Bastiaansen et al., 2005), we also examined how context can affect reading words of different classes.

The main finding of the study was a greater power decrease in the alpha-band for OC than CC words; this effect spanned 200–600 ms over left frontal and right posterior areas. While power increases in the theta and gamma bands typically reflect active processing, the opposite is true for the alpha frequency range. Here, power decreases are generally thought to reflect more cortical processing or engagement (e.g., Jokisch and Jensen, 2007; Klimesch et al., 2007). As OC words carry more lexical-semantics than CC words, reading OC words involves more lexical-semantic retrieval. Thus our results support the notion that alpha power decreases may be related to lexical-semantic retrieval operations. Evidence for this relationship comes from several other studies. In their comparison of OC vs. CC words, Bastiaansen et al. (2005) found not only theta power increases but also significant alpha power decreases between 300 and 500 ms at right posterior channels. The topography of our alpha effect looks remarkably similar to the topography found in their study. This suggests that alpha reflects similar processes in both studies. Studies of semantic judgment tasks have further implicated the involvement of alpha power decreases with semantic processing (Klimesch et al., 1997; Röhm et al., 2001; reviewed in Klimesch, 1999). Evidence from several studies also suggests that alpha power decreases can reflect increased attention (see Klimesch, 1999 for a review). It is unlikely that there were greater attentional demands in reading OC words compared with CC words; thus we favor a semantic interpretation for the word class effect.

Given the consistency in the alpha response across studies, it was notable that we did not observe a significant effect in the theta range. The main results from the motivating studies (Bastiaansen et al., 2005, 2008) pointed to theta power increases as involved in lexical-semantic retrieval in a younger population of subjects. In contrast, our data suggest that theta power may not play a role in lexical-semantic processing in an older population. Instead, for older participants, semantic processing mechanisms may rely more on alpha oscillatory dynamics. We want to emphasize that the comparison of these effects across the two different studies is indirect and qualitative at best. Our study cannot speak directly to aging effects in the theta and alpha-bands but rather suggests the existence of aging effects, a suggestion that should be further investigated by a direct comparison between two age groups in a subsequent study. Still a comparison between the studies is warranted as they used similar stimuli (open and closed class words in a sentence context presented at the same duration and rate as our study) and tasks (participants were instructed to read the words and were asked comprehension questions). Two main differences were the inclusion of a second variable in our study, that of context (Bastiaansen et al., 2005 did not present words outside of a sentence context), and the languages of presentation (Dutch vs. English). There is no evidence that oscillatory dynamics differ based on the testing language.

Previous evidence suggests that theta power may decrease with age. Studies of working memory have observed that theta power in older subjects decreases relative to younger subjects (Karrasch et al., 2004; Cummins and Finnigan, 2007). Thus it is possible that we are observing an effect of aging in the shift from theta-band effects to alpha-band effects though this cannot be said with more confidence without younger controls. Ultimately, the previously established theta power increase does not appear to be a robust phenomenon related to lexical-semantic retrieval in all populations. Further work directly comparing these different populations within the same study would lend more support to the hypothesis that decreases in theta power during lexical-semantic processing are related to aging.

The observation that alpha and beta power was smaller for words in a sentence than a scrambled sentence between 0 and 700 ms suggests that context modulates the oscillatory dynamics in these bands. A methodological challenge exists, however, in interpreting this context effect. Since our time–frequency analysis computed all power changes relative to pre-word baselines, the post-word differences observed in the sentence–scrambled sentence contrast may have two possible causes: (1) the processing-related differences of these words, and (2) the processing-related differences in the baseline periods before each open or closed class word. The reason for these baseline differences is that the baseline power in the sentence context is likely to be influenced by sentence-level processes such as syntactic parsing, semantic integration, working memory demands, or even attentional demands. These processes are probably not (or at least to a lesser extent) engaged in the scrambled sentence context which leads to the possible differences in baseline power between sentence and scrambled sentence conditions. Therefore, as this comparison was not ideally controlled, we would feel it misleading to interpret the alpha and beta power changes as specifically reflecting one of these sentence-level processes. Further work with more tightly controlled conditions could help disambiguate the observed context main effects.

The previous study of OC and CC words by Bastiaansen et al. (2005) only included words within a sentence context; thus it was not clear if the observed effects solely reflected word-level processing or may include sentence-level processing also. In order to examine how reading words of different class may be affected by context, we inspected the interaction between these factors. We followed up the marginally significant interaction with simple effects tests of OC–CC in the scrambled sentence context and OC–CC in the sentence context and only found a significant effect for the contrast in the scrambled sentence context. Thus the class effect observed in the scrambled sentence context does not show up in the sentence context. This might indicate that the main effect of class is driven mainly by words in the scrambled sentence context and therefore primarily reflects word retrieval mechanisms. But alpha power decreases are present in both main effects of word class and context which suggests that alpha is driven by both word retrieval and sentence processing. We tentatively propose that an interaction between word class and context arises because the class effect is being obscured by sentence-level processing such that it is not seen in the sentence context. As mentioned above, alpha power decreases have been previously linked to attentional processing (see Klimesch, 1999 for a review). Thus one possibility is that larger attention-related alpha decreases in the sentence context may make it difficult to reliably detect the additional alpha decreases due to word class differences, at least not as clearly as observed in the scrambled sentence context. Thus greater attentional allocation during sentence reading than during scrambled sentence reading may be “swamping” the class effect.

Additionally, we wanted to extend the previous study on OC vs. CC words (Bastiaansen et al., 2005) by examining potential effects in the gamma frequency band (i.e., above 30 Hz). However, we did not observe significant gamma power changes between OC and CC words. Since a relationship between gamma power increases and sentence-level semantic unification/integration has previously been observed (Hagoort et al., 2004; Hald et al., 2006; Pena and Melloni, 2011), this absence of gamma band effects might suggest that processing lexical-semantics relies partly on different neuronal mechanisms from processing sentence-level semantics. The current literature suggests that the neuronal dynamics of lexical-semantic processing may be confined to the lower frequencies, as opposed to previously observed sentence-level semantic processes which are situated in the gamma frequency range. However, more work is needed to further substantiate such a claim.

Several potential confounds exist in this study. In comparing OC and CC words to examine differences in semantic content, it must be remembered that these word classes naturally have different frequencies and lengths. While we did see significant differences in both frequency and length, evidence is currently lacking that these variables affect oscillatory dynamics. Bastiaansen et al. (2005) did not find that word frequency influenced the amplitude of oscillatory responses. Thus, it is probably unlikely that any word frequency difference would influence our power results. Another potential confound is repetition effects as we had more repetitions for CC words than OC words. We did try to minimize this repetition and maximize exposure to a variety of CC words by including 69 unique CC words, but more repetition for CC words naturally reflects the higher word frequency of CC words. To our knowledge, there are no published reports of repetition effects on oscillatory dynamics during visual word processing with repetition lags greater than one (as we had here).

We observed a word class effect only in the alpha-band in a sample of older subjects. Thus the previously observed word class effects on theta power changes in a younger participant sample do not seem to be a robust effect across populations of different age. This suggests that there may be different neuronal dynamics during word retrieval for different populations. Moreover, the interaction between word class and context suggests that there is an interaction of word retrieval mechanisms with sentence-level comprehension mechanisms in the alpha-band.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.