The functional dissociation of posterior parietal regions during multimodal memory formation

Abstract

The incidental acquisition of multimodal associations is a key memory function for everyday life. While the posterior parietal cortex has been frequently shown to be involved for these memory functions, ventral and dorsal regions revealed differences in their functional recruitment and the precise difference in multimodal memory processing with respect to the associative process has not been differentiated. Using an incidental multimodal learning task, we isolated the associative process during multimodal learning and recollection. The result of the present functional magnetic resonance imaging (fMRI) study demonstrated that during both learning and recollection a clear functional differentiation between ventral and dorsal posterior parietal regions was found and can be related directly to the associative process. The recruitment of a ventral region, the angular gyrus, was specific for learning and recollection of multimodal associations. In contrast, a dorsal region, the superior parietal lobule, could be attributed to memory guided attentional processing. Independent of the memory stage, we assumed a general role for the angular gyrus in the generation of associative representations and updating of fixed association, episodic memory.

Keywords: fMRI; memory; mulitmodal.

FIGURE 1

Schematic illustration of the experimental paradigm: the paired‐associate learning task and the completion task combined with a confidence rating. In the learning phase, participants were instructed to react to new audiovisual stimulus pairs (e.g., a picture of an owl and a sound of a car). Unbeknownst to the participants, audiovisual pairs were divided into two different conditions comprising of an equal number of auditory and visual stimuli. The conditions differed in their underlying associative regularity determining how unimodal stimuli were bound into audiovisual pairs. Unimodal stimuli of the first categorical condition were assigned into fixed audiovisual pairs, which were consistently presented together throughout learning (fixed association condition). In the second categorical condition, unimodal stimuli were continuously recombined into different audiovisual pairs (variable association condition). Importantly, each unimodal stimulus was presented an equal amount of times across conditions. For the recollection phase, we used a completion task combined with a confidence rating task as a reliable measure for the amount of acquired multimodal knowledge

FIGURE 2

Behavioral results. The more pronounced decrease in reaction times (RTs) across learning sessions (divided in six sub‐sessions) for the fixed association (red) condition compared to the variable association (blue) condition demonstrates fast processing of incoming information based on stable multimodal associations. Error bars indicate standard deviations

FIGURE 3

Activation in the left angular gyrus and recollection strength of multimodal information. The correlation between the maximal signal intensity within the left angular gyrus (AnG) and the behavioral measure (d′) of each participant is plotted. It revealed a positive correlation between memory sensitivity and increased activations in the left AnG (Pearson correlation; r ∼ = .73 and p <.001). Only statistical clusters after a small volume corrected (SVC) were shown in the corresponding regions‐of‐interest (ROIs) (display voxel threshold: p <.05, SVC). Dots are single‐subject values. The dotted line represents the linear regression line, indicating the extent of correlation between the two variables on the vertical and horizontal axes

FIGURE 4

Different functional roles for the ventral and dorsal posterior parietal cortex during the acquisition of multimodal knowledge. We found increased activation in the left angular gyrus (AnG) for the contrast fixed association > variable association (upper left panel, activation in red), and increased activation in the left SPL for the contrast variable association > fixed association (upper right panel, activation in blue). Only statistical clusters after a SVC were shown in the corresponding ROIs (display voxel threshold: p <.05, SVC). For visualization, we extracted the mean contrast estimates at the peak coordinate in the left AnG (x = −48, y = −70, z = 32) and left SPL (x = −32, y = −54, z = 36) across session and each condition, respectively. A linear function (regression) was fitted to the extracted data to reveal the neural effects of multimodal learning across session and condition. Line graphs represent the multimodal learning‐related effects between the factors condition (red: fixed association condition, blue: variable association condition) and session. Lower left panel: For the fixed association condition, AnG activity increased during learning of fixed association multimodal material in comparison to the variable association material. Lower right panel: In contrast, fMRI signal increased within the left SPL during learning of variable association multimodal associations but decreased for fixed association associations. Error bars indicate standard error of the mean (SEM)

FIGURE 5

Increased activity within bilateral hippocampus during multimodal learning. For both multimodal conditions, fixed association (red) and variable association (blue), neural activity increased in right and left hippocampal structures (left hippocampus: fixed association: x = −26, y = −12, z = −14; variable association: x = −28, y = −12, z = −14; right hippocampus: fixed association: x = 30, y = −22, z = −14; variable association: x = 28, y = −22, z = −14), revealing its involvement in the flexible acquisition and organization of multimodal relational information. Display voxel threshold: p <.05, SVC

FIGURE 6

Recollection‐related effects in ventral and dorsal regions of the parietal cortex. Upper panel (activation in red): The retrieval of fixed association multimodal associations was related to increased activity within ventral regions of the parietal cortex, in bilateral angular gyrus (AnG) (MNI coordinates: left: x = −40, y = −74, z = 32; right: x = −52, y = −58, z = 16). Lower panel (activation in blue): Increased activity within dorsal regions of the parietal cortex, in bilateral superior parietal cortex (MNI coordinates: left: x = −28, y = −52, z = 40; T = 6.57; right: x = 48, y = −62, z = 44), was associated with the recollection of variable association multimodal associations. Display voxel threshold: p <.05, small volume corrected