Language Tasks and the Network Control Role of the Left Inferior Frontal Gyrus

Abstract

Recent work has combined cognitive neuroscience and control theory to make predictions about cognitive control functions. Here, we test a link between whole-brain theories of semantics and the role of the left inferior frontal gyrus (LIFG) in controlled language performance using network control theory (NCT), a branch of systems engineering. Specifically, we examined whether two properties of node controllability, boundary and modal controllability, were linked to semantic selection and retrieval on sentence completion and verb generation tasks. We tested whether the controllability of the left IFG moderated language selection and retrieval costs and the effects of continuous θ burst stimulation (cTBS), an inhibitory form of transcranial magnetic stimulation (TMS) on behavior in 41 human subjects (25 active, 16 sham). We predicted that boundary controllability, a measure of the theoretical ability of a node to integrate and segregate brain networks, would be linked to word selection in the contextually-rich sentence completion task. In contrast, we expected that modal controllability, a measure of the theoretical ability of a node to drive the brain into specifically hard-to-reach states, would be linked to retrieval on the low-context verb generation task. Boundary controllability was linked to selection and to the ability of TMS to reduce response latencies on the sentence completion task. In contrast, modal controllability was not linked to performance on the tasks or TMS effects. Overall, our results suggest a link between the network integrating role of the LIFG and selection and the overall semantic demands of sentence completion.

Figure 1.

Overview of methods. A, cTBS was administered to each subject’s pars triangularis (pictured with the bullseye) or the cranial vertex. B, Diffusion tractography was computed for each subject. A cortical parcellation was registered to each individual’s anatomic T1 image to identify anatomic divisions. C, A region × region anatomic adjacency matrix was constructed representing the streamline counts between pairs of regions corrected for region volume. D, We applied a community detection algorithm to identify an initial consensus partition based on partitions identified within subjects. E, Modal and boundary controllability were computed for each node (brain region) in the network for each individual. Each node received a rank representing its strength of control within the individual. F, Maps representing the variability in modal controllability (top) and boundary controllability (bottom). P_1…N represent different participants. The relationship between controllability values at the LIFG stimulation site and task RTs before and after stimulation were examined using mixed effects models.

Figure 2.

Selection and retrieval demands within the tasks. Items with high selection and low retrieval demands are those with many highly associated responses, and items with low selection and high retrieval demands are those with one weakly associated response. The stimuli were either verb cues in the verb generation task, or sentence cues in the sentence completion task. Even if selection and retrieval demands are similar in LSAs, each task places different predictive and syntactic demands on the semantic system that could influence performance. Selection and retrieval demands were measured continuously in a relative semantic space using LSA entropy and association strength, respectively, computed at the item level separately for each task.

Figure 3.

Selection and retrieval costs differ across language tasks. Selection costs were higher during the sentence completion task, whereas retrieval costs were higher in the verb generation task.

Figure 4.

Boundary controllability moderates selection costs during sentence completion. Increased entropy values are associated with higher selection demands. A steeper positive slope of the relationship between entropy and RTs represents higher selection costs. Selection costs were higher at baseline in individuals with higher boundary controllability. To visualize the effects of the continuous boundary controllability values as a third dimension, we used a split of estimated regression lines from the models at −1 and 1 SDs of boundary controllability across the sample at baseline. For the exact model estimates for the main effects of entropy and LIFG boundary controllability and their interaction, see Table 5. SD, standard deviation.

Figure 5.

TMS Effects. In the sham group, responses on sentence completion slowed, whereas responses on verb generation slightly quickened. Inhibitory TMS improved sentence completion performance relative to sham.

Figure 6.

LIFG boundary controllability moderates TMS effects. TMS effects were moderated by LIFG boundary controllability specifically in sentence completion, where a crossover interaction was observed. Inhibitory TMS in individuals with higher boundary controllability attenuated the slowed performance observed pre-TMS among the active subjects. However, in verb generation, changes in RTs were consistently related to baseline performance in both the active and sham condition. Boundary controllability is plotted as the zero-centered rank controllability values at the LIFG across the sample. See Extended Data Figure 6-1 illustrating baseline differences in boundary controllability values between the active and sham groups. See Extended Data Figure 6-2 for a plot of all raw RT distributions by group, session, task, and selection and retrieval demands. See also Extended Data Figures 6-3 and 6-4 for trialwise modeling effects.