A Dual Role for the Dorsolateral Prefrontal Cortex (DLPFC) in Auditory Deviance Detection

Abstract

Background: In the oddball paradigm, the dorsolateral prefrontal cortex (DLPFC) is often associated with active cognitive responses, such as maintaining information in working memory or adapting response strategies. While some evidence points to the DLPFC's role in passive auditory deviance perception, a detailed understanding of the spatiotemporal neurodynamics involved remains unclear.

Methods: In this study, event-related optical signals (EROS) and event-related potentials (ERPs) were simultaneously recorded for the first time over the prefrontal cortex using a 64-channel electroencephalography (EEG) system, during passive auditory deviance perception in 12 right-handed young adults (7 women and 5 men). In this oddball paradigm, deviant stimuli (a 1500 Hz pure tone) elicited a negative shift in the N1 ERP component, related to mismatch negativity (MMN), and a significant positive deflection associated with the P300, compared to standard stimuli (a 1000 Hz tone).

Results: We hypothesize that the DLPFC not only participates in active tasks but also plays a critical role in processing deviant stimuli in passive conditions, shifting from pre-attentive to attentive processing. We detected enhanced neural activity in the left middle frontal gyrus (MFG), at the same timing of the MMN component, followed by later activation at the timing of the P3a ERP component in the right MFG.

Conclusions: Understanding these dynamics will provide deeper insights into the DLPFC's role in evaluating the novelty or unexpectedness of the deviant stimulus, updating its cognitive value, and adjusting future predictions accordingly. However, the small number of subjects could limit the generalizability of the observations, in particular with respect to the effect of handedness, and additional studies with larger and more diverse samples are necessary to validate our conclusions.

Keywords: BA 46; BA 8; P300; frequency-domain fNIRS; mismatch negativity; oddball paradigm; optical imaging.

Figure 1

Schematic representation of the co-localization of the 8 light detectors (red circles) and 22 light sources (blue squares) over prefrontal and premotor areas of the cerebral cortex and the 64-channel EEG setup according to the International 10/20 system.

Figure 2

(A) Grand–average waveforms of the ERPs evoked by standard (dashed blue) and deviant (red) tones (mean$\pm 2\times$ SEM) at locations corresponding to 9 sets of electrodes along the antero-posterior and mesio-lateral axis. Four ERP components (N1, N2, P3a, and P3b) were identified. (B) Topographic maps of the consistency of differential activations (contrast analysis between deviant and standard tone conditions) for N1, N2, P3a, and P3b ERP components. The contour lines connect the points with the same value of consistency of differential activation.

Figure 3

Differential activations in the event–related optical signals (EROS) following a contrast analysis (deviant tone > standard tone, Z-score $>2.575$, n > 10. (A) Raw EROS data analysis. The upper panels show the axial projection of the Z-score surface maps (computed across subjects) on a template MRI for the contrast analysis at 88, 120, and $320\mathrm{ms}$ after stimulus onset. The Talairach coordinates x and y of the voxels with the greatest differential activation are indicated with the corresponding Brodmann area (BA) and nearest cortical gyri. The corresponding Talairach z coordinate is on the cortical surface. The lower panels show the corresponding EROS grand–average curves (mean $\pm 2\times$SEM), from $100\mathrm{ms}$ before stimulus onset to $600\mathrm{ms}$ after stimulus onset. of the peak voxel and its direct neighboring voxels during the deviant (red) and the standard (dashed blue) tones conditions. An arrow indicates the timing of the greatest differential activation with a sign (n.s.) not significant and (*) $p<0.05$, for the significance level of the differential activation at the peak latency with multiple comparison correction within the associated ROI. (B) Standardized EROS data analysis. The upper panels show the axial projection of the new Z-score surface maps (computed across subjects) on a template MRI recomputed following the standardization procedure described in the Methods Section 2.4, for the contrast analysis at 88, 128, and $320\mathrm{ms}$ after stimulus onset. At $88\mathrm{ms}$, no voxel of the differential activation reached the threshold level Z-score $>2.575$, n > 10. At 128 and $320\mathrm{ms}$ after stimulus onset, the Z-score of the differential activations was above the threshold level and remained significant ($p<0.05$) even after multiple comparison correction within the associated ROI.