Dissociated Roles of the Inferior Frontal Gyrus and Superior Temporal Sulcus in Audiovisual Processing: Top-Down and Bottom-Up Mismatch Detection

<div><p>Visual inputs can distort auditory perception, and accurate auditory processing requires the ability to detect and ignore visual input that is simultaneous and incongruent with auditory information. However, the neural basis of this auditory selection from audiovisual information is unknown, whereas integration process of audiovisual inputs is intensively researched. Here, we tested the hypothesis that the inferior frontal gyrus (IFG) and superior temporal sulcus (STS) are involved in top-down and bottom-up processing, respectively, of target auditory information from audiovisual inputs. We recorded high gamma activity (HGA), which is associated with neuronal firing in local brain regions, using electrocorticography while patients with epilepsy judged the syllable spoken by a voice while looking at a voice-congruent or -incongruent lip movement from the speaker. The STS exhibited stronger HGA if the patient was presented with information of large audiovisual incongruence than of small incongruence, especially if the auditory information was correctly identified. On the other hand, the IFG exhibited stronger HGA in trials with small audiovisual incongruence when patients correctly perceived the auditory information than when patients incorrectly perceived the auditory information due to the mismatched visual information. These results indicate that the IFG and STS have dissociated roles in selective auditory processing, and suggest that the neural basis of selective auditory processing changes dynamically in accordance with the degree of incongruity between auditory and visual information.</p></div

Behavioral results.

<p>Average percentages of trials with accurate recognition of target auditory information were 100% (SE = 0.00%), 31.6% (SE = 11.0%) and 46.7% (SE = 13.9%) in the congruent, low-incongruent and high-incongruent conditions, respectively, A two-tailed paired t-test revealed that all the differences were significant (false-discovery rate correction, p < 0.05). Error bars indicate standard error of the mean.</p

Experimental details.

<p>Patients were shown movie clips in which a Japanese female produced a lip movement of “pa,” “ka,” “ta,” or “su” with a voice speaking the syllable of “pa,” “ka,” or “ta.” In the congruent condition, the syllable spoken by the voice was congruent with the lip movement. In the incongruent conditions, the audiovisual information was mismatched: In the low-incongruent condition the voice “pa” was presented with the lip movement “ka” and in the high-incongruent condition the voice “pa” was presented with the lip movement “su”. A fixation point was presented for between 500 and 1500 ms before the onset of the movie clip. The interval between the onset of the movie clip and the onset of the audio was 1000 ms. The total length of each movie clip was 2500 ms.</p

Temporal dynamics of high gamma activity (HGA).

<p>The percentage changes of HGA in the inferior frontal gyrus and superior temporal sulcus are calculated in the congruent (blue) and incongruent (red) conditions, respectively. Shading means the standard error of mean. N represents the number of trials. The horizontal black bar indicates the epoch in which the increase in HGA was greater in the incongruent conditions than in the congruent condition (p < 0.0001). The results suggest that audiovisual mismatch increased HGA in later period (500–1000 ms after voice onset).</p

A representative result of time-frequency analysis (patient 3).

<p>The result indicates that the neural activity for processing audiovisual mismatch appeared mainly in the high gamma band (70–150Hz).</p

Relation between high gamma activity (HGA) and voice perception.

<p>Across all electrodes of all patients, average standard increases in HGA were statistically compared between success and error trials. In the inferior frontal gyrus (IFG), the voice-induced standardized increase in HGA was significantly higher in correct trials than in incorrect trials in the low-incongruent condition (p = 4.76E-9, two-tailed paired t-test). In the superior temporal sulcus (STS), the voice-induced standardized increase in HGA was significantly higher in correct trials than in incorrect trials in the high-incongruent condition (p = 0.0291, two-tailed paired t-test). N represents the number of electrodes in the IFG and STS. The y axis shows the average percentage of standardized power change in HGA. Error bars indicate standard error of the mean.</p

Distribution maps of the high gamma activity (HGA).

<p>All the electrodes with a significantly greater HGA increase in the incongruent condition than in the congruent condition are shown on a template brain in the low-incongruent (upper) and high-incongruent (lower) conditions. The shapes of the electrode markers indicate individual patients. The bar charts beside the template brain image show the average percentage of electrodes that showed a significant HGA increase in the inferior frontal gyrus (IFG; orange), superior temporal sulcus (STS; purple), and other (gray) regions respectively. In the early period, in both the low- and high-incongruent conditions, only a few of the 1054 electrodes exhibited a significant HGA increase (left). In the later period, more electrodes showed a significant HGA increase. The increase was localized in the IFG in the low-incongruent condition (p = 0.0462; right upper) and in the STS in the high-incongruent condition (p = 0.0254; right lower). Error bars indicate standard error of the mean.</p

Additional file 1: Table S1. of Genetic and epigenetic stability of oligodendrogliomas at recurrence

Clinical characteristics of the patient cohort. Table S2. Sequence data summary. Table S3. List of the somatic mutations in this study. (XLSX 163 kb

Additional file 2: Figure S1. of Genetic and epigenetic stability of oligodendrogliomas at recurrence

Histopathological features of primary and recurrent tumors in a 34 year-old female (patient 6). The primary tumor was diagnosed as anaplastic oligodendroglioma (WHO grade III) (A). Postoperatively, the patient was treated with 8 courses of PAV chemotherapy. Eight years after the initial surgery, an MRI FLAIR-high lesion was noticeably enlarged and this region showed high uptake in Methionine PET. Tumor recurrence was therefore suspected and surgical resection was performed. In the recurrent tumor, atypia of the nucleus was improved and numbers of mitotic cells were decreased compared to the primary tumor, and the tumor was diagnosed as oligodendroglioma (WHO grade II) (B). Formalin-fixed paraffin-embedded tissues were sectioned and stained with Hematoxylin and Eosin (bar = 100 μm). Figure S2. Histopathological features of different tumor portions from the same patient as listed in Additional file 1: Table S1. Formalin-fixed paraffin-embedded tissues were sectioned and stained with Hematoxylin and Eosin (bar = 100 μm). A. Patient 13, Methionine PET low uptake, grade II; B. Patient 13, Methionine PET high uptake, grade III; C. Patient 14, Gadolinium enhanced -, grade II; D. Patient 14, Gadolinium enhanced +, grade III; E. Patient 15, Methionine PET low uptake, grade II; F. Patient 15, Methionine PET high uptake, grade II; G. Patient 16, Methionine PET low uptake, grade III; H. Patient 16, Methionine PET high uptake, grade III. (PPTX 1597 kb

Additional file 2: Table S1. of A combination of TERT promoter mutation and MGMT methylation status predicts clinically relevant subgroups of newly diagnosed glioblastomas

Molecular and clinical characteristics of Cohort 1 (n = 758). Table S2. Molecular and clinical characteristics of GBM cohort (n = 453). Table S3. Univariate and multivariate Cox regression analyses for Group A (IDH mutated-TERT mutated) tumors in Cohort 1 (n = 155). Table S4. Univariate and multivariate Cox regression analyses for Group B (IDH mutated-TERT wild-type) tumors in Cohort 1 (n = 131). Table S5. Univariate and multivariate Cox regression analyses for Group C (IDH wild-type-TERT wild-type) tumors in Cohort 1 (n = 237). Table S6. Univariate and multivariate Cox regression analyses for Group D (IDH wild-type-TERT mutated) tumors in Cohort 1 (n = 235). Table S7. Univariate and multivariate Cox regression analyses for GBM in Cohort 1 (n = 260). Table S8. Univariate and multivariate Cox regression analyses for GBM in Cohort 2 (n = 193). Table S9. Background of combined GBM cohort stratified by TERT and MGMT status (n = 453). Table S10. Survival time and WHO grade in each molecular subgroup of Cohort 1 (n = 758). (XLSX 254 kb