Theta Oscillations and Source Connectivity During Complex Audiovisual Object Encoding in Working Memory

Abstract

Working memory is a limited capacity memory system that involves the short-term storage and processing of information. Neuroscientific studies of working memory have mostly focused on the essential roles of neural oscillations during item encoding from single sensory modalities (e.g., visual and auditory). However, the characteristics of neural oscillations during multisensory encoding in working memory are rarely studied. Our study investigated the oscillation characteristics of neural signals in scalp electrodes and mapped functional brain connectivity while participants encoded complex audiovisual objects in a working memory task. Experimental results showed that theta oscillations (4-8 Hz) were prominent and topographically distributed across multiple cortical regions, including prefrontal (e.g., superior frontal gyrus), parietal (e.g., precuneus), temporal (e.g., inferior temporal gyrus), and occipital (e.g., cuneus) cortices. Furthermore, neural connectivity at the theta oscillation frequency was significant in these cortical regions during audiovisual object encoding compared with single modality object encoding. These results suggest that local oscillations and interregional connectivity via theta activity play an important role during audiovisual object encoding and may contribute to the formation of working memory traces from multisensory items.

Keywords: EEG; audiovisual object; encoding; functional connectivity; theta; working memory.

Figure 1

Schematic of the experimental task. A three-block design was used in the behavioral experiment. In each three-block trial, a fixation cross was shown for 0.5 s; a stimulus (visual-V, auditory-A, or congruent audiovisual-AV) was then presented for 0.6 s; a blank screen was shown for 2 s; and finally, the test stimulus appeared for 0.6 s with a 3-s time limit.

Figure 2

Statistical results of behavioral data. (A) Comparisons of RT for memory retrieval among the three conditions (V, A, and AV). (B) Comparisons of power spectral density in theta frequency among the three conditions (V, A, and AV) during the encoding phase of working memory processing (0–600 ms). The error bar presents the standard error of the mean. ^*p < 0.05; ^***p < 0.001.

Figure 3

The power spectrum density of frequencies (peak at theta band around 5 Hz) across the three encoding conditions (A, V, and AV). The shaded area denotes the standard deviation.

Figure 4

Group-averaged time-frequency spectra during the three conditions (V, A, and AV) and comparisons of the conditions (AV vs. V and AV vs. A). Time (in seconds) is denoted on the x-axis, with 0 s defined as the onset of the encoding stimulus. Frequency (in Hz) is shown on the y-axis. All signal power data are expressed in a logarithmic scale, with the color legend shown to the far right (unit: dB). Statistical values (t values) of time-frequency representation comparisons of the conditions are also shown with the color legend at the bottom. The top panel shows that theta activity increased during the encoding stage (110–270 ms) across the three conditions (V, A, and AV). The bottom panel, marked with a black box, shows the differences in theta activity between the AV and V conditions and between AV and A.

Figure 5

Statistical maps of source locations at theta frequency were projected onto a three-dimensional brain MRI template (top panel) and fiducial cortical surface (bottom panel). Non-parametric permutation test statistical analysis was performed to compare the current density distributions of AV with A + V. Colored areas represent the spatial extent of voxels with a significant difference in the current density. Log-F-ratio statistics were applied, and the color scale represents log-F-ratio values (threshold log-F-ratio = 3.36, p < 0.05). The MRI slices are located at MNI-space coordinates. In the averaged time windows of theta activity (110–260 ms), the maximum current density differences were found in the left superior frontal gyrus (Brodmann area 8, MNI: −30 20 50), right precuneus (Brodmann area 7, MNI: 5 −40 45), right inferior temporal gyrus (Brodmann area 21, MNI: 65 −15 −20), right cuneus (Brodmann area 18, MNI: 20 −95 20). The color scale represents the log-F-ratio values of current source density (threshold: log-F-ratio = 3.36, p < 0.05). A, anterior; P, posterior; S, superior; I, inferior; L, left; R, right.

Figure 6

Wire diagram showing significant FC differences between AV and A conditions and between AV and A+V (|t|_min > 3.73, p < 0.05) (blue and red wires) based on physiological lagged connectivity measures by cortical eLORETA signals. These results correspond to theta oscillations (4–8 Hz). The red wire denotes increased connectivity; the blue wire denotes decreased connectivity. L, left; R, right; SFG, superior frontal gyrus; ITG, inferior temporal gyrus.