Sense of self impacts spatial navigation and hexadirectional coding in human entorhinal cortex

Grid cells in entorhinal cortex (EC) encode an individual’s location in space and rely on environmental cues and self-motion cues derived from the individual’s body. Body-derived signals are also primary signals for the sense of self and based on integrated sensorimotor signals (proprioceptive, tactile, visual, motor) that have been shown to enhance self-centered processing. However, it is currently unknown whether such sensorimotor signals that modulate self-centered processing impact grid cells and spatial navigation. Integrating the online manipulation of bodily signals, to modulate self-centered processing, with a spatial navigation task and an fMRI measure to detect grid cell-like representation (GCLR) in humans, we report improved performance in spatial navigation and decreased GCLR in EC. This decrease in entorhinal GCLR was associated with an increase in retrosplenial cortex activity, which was correlated with participants’ navigation performance. These data link self-centered processes during spatial navigation to entorhinal and retrosplenial activity and highlight the role of different bodily factors at play when navigating in VR.

Bodily self and human grid cell-like activity: probing spatial representation with immersive virtual reality

Hyukjun Moon

Grid cells are place-modulated neurons that encode the location of an agent in space, relying on the integration of various sensorimotor signals from the body. Of note, the integration of those signals is also fundamental for the agent's conscious experience of selfhood, referred to as bodily self-consciousness (BSC). Although both grid cells and BSC systems are related to the brain mechanisms of self-location and are based on multimodal signal integration, their interplay has never been investigated. My thesis aimed at revealing their links in humans by assessing the impact of BSC modulations on grid cell-like representation (GCLR): an fMRI proxy of grid cell activity in entorhinal cortex (EC). In Study 1, I assessed whether manipulation on BSC, specifically enhancing self-identification, affects GCLR during spatial navigation in a virtual reality (VR) environment. I implemented a novel fMRI paradigm integrating a spatial navigation task with online BSC manipulation through a motion-mimicking avatar. The data showed a significant reduction of GCLR as well as improved spatial navigation performance in the condition with the self-identified avatar, linking entorhinal grid cell activity and BSC through bodily self-motion cues provided online during spatial navigation. These behavioral and neural changes were further associated with increased activity in posterior parietal and retrosplenial cortex, collectively suggesting the impact of BSC on a distributed spatial navigation networks in the human brain. Consistent with the previous BSC research, in Study1, I observed illusory drifts in experienced self-location toward the self-identified avatar. In Study2, I further investigated whether illusory self-location changes would be sufficient to elicit GCLR in the absence of active spatial navigation. Adopting the Full-body illusion (FBI) paradigm to the MRI scanner, my data extend changes in self-location related to multisensory stimulation and demonstrated that these indeed evoke GCLR. Although the amplitude of GCLR during the FBI was smaller than the one during virtual navigation, their grid orientations were similar. These data suggest that the brain mechanisms underlying the BSC-induced illusory self-location are similar and comparable, albeit weaker, to the ones during virtual navigation.Temporal Interference (TI) stimulation is a novel method that can excite or inhibit neurons in the deep brain by combining high-frequency electrical fields. Building on the previous studies, in study3, I probed the causal link between GCLR and spatial navigation by applying TI stimulation to EC of participants while they were performing a VR navigation task in the scanner. The preliminary results showed that their spatial navigation was improved by excitatory stimuli compared to the control, while it deteriorated during the inhibition. Besides, I found that modulated GCLR was also associated with improved performance in the excitatory condition. Together, these data provide the first causal link between GCLR and spatial navigation, showing potential future avenues for navigation enhancement in humans. To summarize, I investigated BSC and grid cell systems jointly in humans and, for the first time, uncovered their links through robust evidence based on both behavioral and neuroimaging data. My thesis shed new light on the research of both systems which are closely intermingled but have hitherto been considered separately.

EPFL2021

Hippocampal Contribution to Ordinal Psychological Time in the Human Brain

Baptiste Gauthier

The chronology of events in time-space is naturally available to the senses, and the spatial and temporal dimensions of events entangle in episodic memory when navigating the real world. The mapping of time-space during navigation in both animals and humans implicates the hippocampal formation. Yet, one arguably unique human trait is the capacity to imagine mental chronologies that have not been experienced but may involve real events-the foundation of causal reasoning. Herein, we asked whether the hippocampal formation is involved in mental navigation in time (and space), which requires internal manipulations of events in time and space from an egocentric perspective. To address this question, we reanalyzed a magnetoencephalography data set collected while participants self-projected in time or in space and ordered historical events as occurring before/after or west/east of the mental self [Gauthier, B., Pestke, K., & van Wassenhove, V. Building the arrow of time horizontal ellipsis Over time: A sequence of brain activity mapping imagined events in time and space.Cerebral Cortex,29, 4398-4414, 2019]. Because of the limitations of source reconstruction algorithms in the previous study, the implication of hippocampus proper could not be explored. Here, we used a source reconstruction method accounting explicitly for the hippocampal volume to characterize the involvement of deep structures belonging to the hippocampal formation (bilateral hippocampi [hippocampi proper], entorhinal cortices, and parahippocampal cortex). We found selective involvement of the medial temporal lobes (MTLs) with a notable lateralization of the main effects: Whereas temporal ordinality engaged mostly the left MTL, spatial ordinality engaged mostly the right MTL. We discuss the possibility of a top-down control of activity in the human hippocampal formation during mental time (and space) travels.

MIT PRESS2020

Bodily self and human grid cell-like activity: probing spatial representation with immersive virtual reality

Hyukjun Moon

EPFL2021

Hippocampal Contribution to Ordinal Psychological Time in the Human Brain

Baptiste Gauthier

MIT PRESS2020