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. 2011 Feb 23;31(8):2801-14.
doi: 10.1523/JNEUROSCI.5003-10.2011.

Simple composition: a magnetoencephalography investigation into the comprehension of minimal linguistic phrases

Affiliations

Simple composition: a magnetoencephalography investigation into the comprehension of minimal linguistic phrases

Douglas K Bemis et al. J Neurosci. .

Abstract

The expressive power of language lies in its ability to construct an infinite array of ideas out of a finite set of pieces. Surprisingly, few neurolinguistic investigations probe the basic processes that constitute the foundation of this ability, choosing instead to focus on relatively complex combinatorial operations. Contrastingly, in the present work, we investigate the neural circuits underlying simple linguistic composition, such as required by the minimal phrase "red boat." Using magnetoencephalography, we examined activity in humans generated at the visual presentation of target nouns, such as "boat," and varied the combinatorial operations induced by its surrounding context. Nouns in minimal compositional contexts ("red boat") were compared with those appearing in matched non-compositional contexts, such as after an unpronounceable consonant string ("xkq boat") or within a list ("cup, boat"). Source analysis did not implicate traditional language areas (inferior frontal gyrus, posterior temporal regions) in such basic composition. Instead, we found increased combinatorial-related activity in the left anterior temporal lobe (LATL) and ventromedial prefrontal cortex (vmPFC). These regions have been linked previously to syntactic (LATL) and semantic (vmPFC) combinatorial processing in more complex linguistic contexts. Thus, we suggest that these regions play a role in basic syntactic and semantic composition, respectively. Importantly, the temporal ordering of the effects, in which LATL activity (∼225 ms) precedes vmPFC activity (∼400 ms), is consistent with many processing models that posit syntactic composition before semantic composition during the construction of linguistic representations.

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Figures

Figure 1.
Figure 1.
Experimental design. Our design crossed task (composition vs list) and number of words (two vs one). In each trial, participants indicated whether the target picture matched the preceding words. To satisfy this criterion, in the composition task, all preceding words were required to match, whereas in the list task, any matching word sufficed. A total of six colors and 25 shapes were randomly combined and used as stimuli. Half of the target pictures matched, but half did not. Only activity recorded at the matched nouns (“boat”) was analyzed.
Figure 2.
Figure 2.
Behavioral results. Reaction time (A) and accuracy (B) data were submitted to a 2 × 2 repeated-measures ANOVA with task (composition vs list) and number of words (one vs two) as factors. We observed a significant interaction between the two factors for reaction time (F(1,19) = 89.2), with post hoc tests revealing slower responses in the two-word list condition and faster responses in the two-word composition condition compared with matched one-word controls. No significant effects were found for accuracy. ns, Nonsignificant; ***p < 0.001.
Figure 3.
Figure 3.
MEG sensor data. The average evoked response to the critical noun is displayed for each condition: A, two-word composition; B, one-word composition; C, two-word list; D, one-word list. Canonical visual response peaks and field patterns (M100 and M170) (Tarkiainen et al., 1999; Pylkkänen and Marantz, 2003) are visible at ∼100 and 150 ms in all four conditions. Subsequent M250 and M350 peaks and field patterns (Pylkkänen et al., 2002; Pylkkänen and Marantz, 2003) are also present across all four conditions. A typical anterior midline field pattern (Pylkkänen and McElree, 2007) can be seen accompanying a sustained increase in activity from 300 to 500 ms within the two-word composition condition. This field pattern is absent from the other three conditions.
Figure 4.
Figure 4.
ROI results. Localized activity is shown for the five ROIs during the comprehension of the critical nouns, averaged across participants. Shaded regions denote significant clusters of combinatorial activity as identified by a cluster-based permutation test (Maris and Oostenveld, 2007) applied to the entire interval of 0–500 ms. Within the LATL (A), a significant cluster of combinatorial activity was found from 184 to 255 ms (p = 0.039), within which two-word composition activity was significantly greater than one-word composition activity, and activity in the list conditions did not differ. A later cluster of combinatorial activity was found in the vmPFC (B) from 331 to 480 ms (p = 0.014). In this time period, localized activity was again significantly greater for the two-word composition condition compared with the one-word composition condition. No differences in activity were observed in the list task. Within the RATL (C), two significant clusters of time points were identified by the interaction permutation test (184–246 ms, p = 0.008; 329–403 ms, p = 0.004). Across the entire time window spanning these two clusters (184–403 ms), activity in the two-word composition condition was significantly greater than in the one-word condition. However, unlike in the LATL and vmPFC, activity in this region also showed a significant difference between the two one-word conditions during the identified time window (p = 0.041), suggesting a task-related suppression of activity in the one-word composition condition as opposed to an increase in activity during the two-word composition condition. No significant clusters of combinatorial activity were found in either the LIFG (D) or LPTL (E) ROIs. Targeted tests within the composition task alone also failed to find any periods of significantly greater activity in the two-word composition condition compared with the one-word composition condition in either region at any time. ns, Nonsignificant; *p < 0.05, **p < 0.01.
Figure 5.
Figure 5.
Full-brain analyses. Plotted regions denote the difference in average amplitude between two-word and one-word conditions for all space time regions in which two-word activity was reliably greater than one-word activity (p < 0.05, uncorrected) for at least 10 ms over 10 spatial neighbors. For clarity, non-cortical sources have been removed. Results within the composition task (A) conform to our ROI analyses and reveal a clear LATL effect from 150 to 250 ms and a clear vmPFC effect from 300 to 450 ms. A sustained difference in activity can also be seen in the RATL from 100 to 400 ms. Additionally, increased activity was also observed within the left superior parietal lobe throughout much of the time interval. Within the list task (B), relatively modest increases in two-word activity were seen in the right inferior frontal gyrus and left inferior temporal lobe from ∼200 to 300 ms.
Figure 6.
Figure 6.
Sensor analysis results. Each row corresponds to one test from the split-half cross-validation analysis. Waveforms represent the RMS of the sensors corresponding to the dominant field patterns present during the LATL (A, B) and vmPFC (C, D) source space effects. Shaded regions denote significant clusters of combinatorial activity as identified by a cluster-based permutation test (Maris and Oostenveld, 2007). The field pattern from the grand average of the two-word composition condition is shown for each significant cluster. Within the left hemisphere sensors, the first data half (A) produced a significant cluster of combinatorial activity from 195 to 215 ms (p = 0.036), within which two-word composition activity was significantly greater than one-word composition activity, and activity in the list conditions did not differ. In the second data half (B), a significant cluster of combinatorial activity was identified from 220 to 241 ms (p = 0.013) in which two-word composition activity was significantly greater than one-word composition activity, and activity in the list conditions did not differ. Within the frontal sensors, the analysis of the first data half (C) revealed a cluster of combinatorial activity from 396 to 448 ms (p = 0.011). In this time period, sensor activity was again significantly greater for the two-word composition condition compared with the one-word composition condition. No differences in activity were observed in the list task. In the second data half analysis (D), a significant cluster of combinatorial activity was found from 388 to 442 ms (p = 0.050). Again, two-word composition activity was significantly greater than one-word composition activity within this cluster, whereas activity in the list conditions showed no significant differences. ns, Nonsignificant; *p < 0.05; **p < 0.01.

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