Differential contributions of inferior frontal gyrus subregions to sentence processing guided by intonation

Abstract

Auditory sentence comprehension involves processing content (semantics), grammar (syntax), and intonation (prosody). The left inferior frontal gyrus (IFG) is involved in sentence comprehension guided by these different cues, with neuroimaging studies preferentially locating syntactic and semantic processing in separate IFG subregions. However, this regional specialisation has not been confirmed with a neurostimulation method. Consequently, the causal role of such a specialisation remains unclear. This study probed the role of the posterior IFG (pIFG) for syntactic processing and the anterior IFG (aIFG) for semantic processing with repetitive transcranial magnetic stimulation (rTMS) in a task that required the interpretation of the sentence's prosodic realisation. Healthy participants performed a sentence completion task with syntactic and semantic decisions, while receiving 10 Hz rTMS over either left aIFG, pIFG, or vertex (control). Initial behavioural analyses showed an inhibitory effect on accuracy without task-specificity. However, electric field simulations revealed differential effects for both subregions. In the aIFG, stronger stimulation led to slower semantic processing, with no effect of pIFG stimulation. In contrast, we found a facilitatory effect on syntactic processing in both aIFG and pIFG, where higher stimulation strength was related to faster responses. Our results provide first evidence for the functional relevance of left aIFG in semantic processing guided by intonation. The stimulation effect on syntactic responses emphasises the importance of the IFG for syntax processing, without supporting the hypothesis of a pIFG-specific involvement. Together, the results support the notion of functionally specialised IFG subregions for diverse but fundamental cues for language processing.

Keywords: TMS; electric field simulations; prosody; semantics; sentence processing; syntax.

FIGURE 1

Overview of the experimental design with within‐subject factors decision type, focus position, and transcranial magnetic stimulation (TMS) site. Trials of each decision type and focus position were presented pseudo‐randomly within each session. During each session, participants received short TMS bursts (five pulses at 10 Hz, starting 100 ms after the visual onset of the determiner or noun response options) over one of the three TMS sites. The order of TMS site across experimental sessions was counter‐balanced across participants. Circles illustrate the three stimulation sites. ACC, accusative; aIFG, anterior inferior frontal gyrus; FEM, feminine; MASC, masculine; NOM, nominative; pIFG, posterior inferior frontal gyrus

FIGURE 2

Pitch contours and willustrating the difference between subject focus (a) and object focus (b) in the example sentence Yesterday, the policeman arrested the thief (“Gestern hat der Polizist den Dieb verhaftet”). The noun phrase that is placed in contrastive focus bears a pitch accent (indicated by capital letters), whereas it is deaccented in the other condition. Note the difference in pitch increase and intensity in the accented noun phrase as compared to the same noun phrase in the deaccented condition

FIGURE 3

Response times (a) and error rates (b) for each decision type and transcranial magnetic stimulation (TMS) site. In (a), the asterisk indicates a main effect of decision type. The upper and lower bounds of the boxes correspond to the third and first quartiles, respectively. The whiskers represent 1.5 times the interquartile range. In (b), the asterisk indicates the main effect of TMS site (posterior inferior frontal gyrus [pIFG] contrasted to vertex). Error bars reflect ±1 SEM. Lines connect subject‐wise data

FIGURE 4

Electric field simulations revealed differential effects of anterior inferior frontal gyrus (aIFG) and posterior inferior frontal gyrus (pIFG) stimulation on response times. (a) Electric fields induced by transcranial magnetic stimulation (TMS) for the aIFG and pIFG stimulation conditions in a representative sample subject. The white line indicates the border between the parts of the gyrus belonging to cytoarchitectonic regions BA45 (aIFG) and BA44 (pIFG). (b) Response times per task condition plotted in function of the electric field strength in the aIFG and pIFG regions of interest (ROIs). In both ROIs, a significant interaction between field strength and decision type was found. Higher electric field strength in the aIFG led to delayed response times in semantic, but faster response times in syntactic decisions. In the pIFG, higher electric field strength was related to a task‐specific facilitation of responses in syntactic trials, with no significant effect on semantic trials. The lines represent the model estimate (confidence intervals indicated by the shaded area). Dots represent single subject peak electric field strength and mean response time. Note that for each participant, two electric field values are plotted per ROI, obtained from each stimulation session (aIFG and pIFG)