Functional segregation of cortical language areas by sentence repetition

Abstract

The functional organization of the perisylvian language network was examined using a functional MRI (fMRI) adaptation paradigm with spoken sentences. In Experiment 1, a given sentence was presented every 14.4 s and repeated two, three, or four times in a row. The study of the temporal properties of the BOLD response revealed a temporal gradient along the dorsal-ventral and rostral-caudal directions: From Heschl's gyrus, where the fastest responses were recorded, responses became increasingly slower toward the posterior part of the superior temporal gyrus and toward the temporal poles and the left inferior frontal gyrus, where the slowest responses were observed. Repetition induced a decrease in amplitude and a speeding up of the BOLD response in the superior temporal sulcus (STS), while the most superior temporal regions were not affected. In Experiment 2, small blocks of six sentences were presented in which either the speaker voice or the linguistic content of the sentence, or both, were repeated. Data analyses revealed a clear asymmetry: While two clusters in the left superior temporal sulcus showed identical repetition suppression whether the sentences were produced by the same speaker or different speakers, the homologous right regions were sensitive to sentence repetition only when the speaker voice remained constant. Thus, hemispheric left regions encode linguistic content while homologous right regions encode more details about extralinguistic features like speaker voice. The results demonstrate the feasibility of using sentence-level adaptation to probe the functional organization of cortical language areas.

Figure 1

Repetition suppression related to sentence repetition. A: In Experiment 1: sagittal slice at x = −49 mm (standard Talairach coordinates) displaying the regions in which repetition induces a linear decrease in amplitude (blue‐yellow scale), superimposed on the activations to the first sentence (yellow‐red scale). Graphs show the adaptation of the mean BOLD response with sentence repetition at four locations that illustrate the different patterns of responses to sentence repetition. Note also the different shapes of the BOLD responses, with, for example, an earlier peak in the middle STS than in the posterior STS. Coordinates are given in standard Talairach coordinates. B: In Experiment 2: sagittal slice at x = −55 mm (Talairach coordinates) displaying the regions significantly more activated when both parameters, sentences and speakers, varied than when both were repeated (blue‐yellow scale) superimposed on the activations to the first sentence (yellow‐red scale).

Figure 2

Temporal organization of cortical responses to sentences for the first and second presentation of the same sentence. Colors encode the circular mean of the phase of the BOLD response, expressed in seconds relative to sentence onset. Fastest responses, in purple, are visible in Heschl's gyrus, while the slowest responses, in yellow and red, are encountered in Broca's area. A delay in phase is visible along the superior temporal region with a dorsal–ventral and anterior–posterior gradient. The second presentation of a sentence speeds up the phase in all these regions.

Figure 3

Repetition suppression related to speaker and sentence repetition in Experiment 2. A: Graphs, surrounding sagittal slices at x = ±60 mm (standard Talairach coordinates), show the adaptation of the mean BOLD response in the different conditions. The black tracing on each plot represents the duration of the speech stimuli (∼19 s). Several patterns are seen. The superior temporal regions (e.g., −48 mm, −12 mm, 0 mm) are activated and do not adapt, while inferior frontal regions (−40 mm, 24 mm, 0 mm) are inactive. The left STS show adaptation to sentence repetition, even when speakers varied (e.g., −60 mm, −12 mm, −3 mm). Right homologous regions either did not adapt (e.g., 51 mm, −39 mm, 3 mm) or adapted only when the speaker was maintained constant (60 mm, −12 mm, −3 mm). B: Axial slices at z = 0 mm (Talairach coordinates), displaying the clusters activated in the different comparisons.