Sense of own body shapes neural processes of memory encoding and reinstatement

Abstract

How is the fundamental sense of one's body, a basic aspect of selfhood, incorporated into memories for events? Disrupting bodily self-awareness during encoding impairs functioning of the left posterior hippocampus during retrieval, which implies weakened encoding. However, how changes in bodily self-awareness influence neural encoding is unknown. We investigated how the sense of body ownership, a core aspect of the bodily self, impacts encoding in the left posterior hippocampus and additional core memory regions including the angular gyrus. Furthermore, we assessed the degree to which memories are reinstated according to body ownership during encoding and vividness during retrieval as a measure of memory strength. We immersed participants in naturalistic scenes where events unfolded while we manipulated feelings of body ownership with a full-body-illusion during functional magnetic resonance imaging scanning. One week later, participants retrieved memories for the videos during functional magnetic resonance imaging scanning. A whole brain analysis revealed that patterns of activity in regions including the right hippocampus and angular gyrus distinguished between events encoded with strong versus weak body ownership. A planned region-of-interest analysis showed that patterns of activity in the left posterior hippocampus specifically could predict body ownership during memory encoding. Using the wider network of regions sensitive to body ownership during encoding and the left posterior hippocampus as separate regions-of-interest, we observed that patterns of activity present at encoding were reinstated more during the retrieval of events encoded with strong body ownership and high memory vividness. Our results demonstrate how the sense of physical self is bound within an event during encoding, which facilitates reactivation of a memory trace during retrieval.

Keywords: body ownership; fMRI; hippocampus; memories for events; naturalistic stimuli.

Fig. 1

Screenshots of an example video: Hagaparken. Each immersive video involved a first-person view of a mannequin’s body that was continuously stroked with the Styrofoam ball as an event unfolded within the scene (A). Participants watched videos through an HMD and felt strokes on their actual torso either synchronously or asynchronously with the strokes in the video (B). Note that footage from only one eye is shown here. Actual stimuli consisted of two videos taken from slightly different positions corresponding to a left and right eye centered in the middle of the HMD to create a stereoscopic effect. Video stimuli were divided into two carefully matched groups to control for differences in visual, auditory, narrative, and emotional complexity (see Supplementary Material).

Fig. 2

The experimental protocol. (A) During the encoding session, participants viewed immersive 3D videos through an HMD during fMRI scanning. For the first 20 s of each video, either synchronous (12 videos) or asynchronous (12 videos) visuotactile stimulation between the participant’s and mannequin’s body was administered to induce a sense of ownership over the mannequin’s body or reduce/abolish the illusion, respectively. The mannequin’s body was superimposed against a still frame image depicting the location of each video. Next, a unique event took place in front of the mannequin as visuotactile stimulation continued, which lasted a total of 20 additional seconds. Participants were asked to remember as much as possible about each scene. After scanning, participant answered cued recall questions and completed subjective ratings about the videos. (B) One week later, participants retrieved memories for the videos again during fMRI scanning. After participants finished retrieving memories but while they were still lying on the scanner table, we assessed the strength of the full-body illusion induction by measuring SCRs to knife threats embedded within two new videos (one with synchronous, one with asynchronous visuotactile stimulation) and questionnaire measures of the degree of ownership over the mannequin’s body. Participants’ eye movements were tracked as they watched the illusion testing videos. The sense of presence within the immersive scene was also assessed for each condition. Finally, participants answered a new set of cued recall questions and completed the same subjective ratings as in the previous session. SCR = skin conductance response.

Fig. 3

The hippocampal ROI used in the MVPA and RSA, based on MNI coordinates extracted from Bergouignan et al. (2014); X = −27, Y = −31, Z = −11).

Fig. 4

RSA contrast matrices. (A) We created individual subject contrast matrices comparing pattern similarity between encoding and retrieval of the same video where similarity is higher in the synchronous condition (on-diagonal). Videos encoded with the body ownership illusion (synchronous condition) received positive weights (i.e. yellow on-diagonal values), while videos encoded with reduced illusion (asynchronous) received negative weights (i.e. blue on-diagonal values) (B) Same-video correlations (on-diagonal) were weighted according to condition (i.e. synchronous = positive/yellow on-diagonal values, asynchronous = negative/blue on-diagonal values) and factor of interest (e.g. memory vividness). This RSA detects regions where reinstatement is greater for videos encoded with the body ownership illusion and increasing memory vividness. An example contrast matrix from a single participant is shown here.

Fig. 5

(A) The average illusion statement scores were significantly higher following synchronous compared with asynchronous visuotactile stimulation, P = 0.02. (B) The peak magnitudes of SCRs were higher for knife threats experienced during the synchronous compared with asynchronous condition, P = 0.01.

Fig. 6

Average cued recall accuracy was higher at immediate testing compared with delayed testing for central event details (P < 0.001), but not peripheral details.

Fig. 7

Average reliving (A) and belief in memory accuracy (B) ratings were higher at immediate compared with delayed testing, P’s < 0.02.

Fig. 8

The whole brain searchlight analysis decoding illusion condition (synchronous or asynchronous) during encoding of the immersive videos identified several regions previously implicated in the sense of body ownership, including the right premotor cortex (A), bilateral lateral occipital cortex (B), and the left intraparietal sulcus (C). The statistical map was thresholded at q_FDR < 0.05 and overlaid onto the average T1w images of 440 subjects obtained from the WU-Minn HCP dataset (van Essen et al. 2013). Cluster peaks within gray matter and cluster extent thresholds of greater than five voxels are depicted.

Fig. 9

Patterns of activity in posterior parietal and medial temporal lobe regions known to be crucial to successful memory formation predicted body illusion condition (synchronous or asynchronous) during the encoding of the immersive videos in a whole brain searchlight analysis. The regions identified included the left angular gyrus (A), the right hippocampus (B&C), and the right parahippocampal gyrus (C). The statistical map was thresholded at q_FDR < 0.05 and overlaid onto the average T1w images of 440 subjects obtained from the WU-Minn HCP dataset (van Essen et al. 2013). Cluster peaks within gray matter and cluster extent thresholds of greater than five voxels are depicted.

Fig. 10

(A) We extracted beta estimates from the hippocampal ROI, based on coordinates identified by Bergouignan et al. (2014); X = −27, Y = −31, Z = −11), corresponding to the univariate contrast comparing memory retrieval, regardless of condition, to the baseline task. Beta estimates were significantly below zero (P = 0.001), indicating deactivation of the left posterior hippocampus during memory retrieval. The dotted line indicates a null effect (i.e. no effect of retrieval on activity in the hippocampal mask). (B) Memory reinstatement (i.e. encoding-retrieval pattern similarity) was stronger for memories encoded with strong body ownership (synchronous versus asynchronous condition) and increasing levels of vividness in the left posterior hippocampal ROI (x-axis: hippocampus), P = 0.03, and in the larger set of regions that decoded strong versus weak body ownership during encoding, P = 0.01 (x-axis: encoding mask). Pearson correlations, between the neural data extracted from each ROI and the individual contrast matrices specifying stronger reinstatement for memories encoded with strong body ownership and retrieved with high vividness (see Fig. 4B), are significantly greater than zero. The dotted line indicates a null effect (i.e. no encoding-retrieval pattern similarity).