Reenacting our past: on the role of motor cortex in memory re-experiencing

Poster No:

852 

Submission Type:

Abstract Submission 

Authors:

Juliette Boscheron1, Mariana Babo-Rebelo1, Arthur Trivier1, Florian Lance1, Bruno Herbelin1, Dimitri Van De Ville1, Olaf Blanke1

Institutions:

1École polytechnique fédérale de Lausanne (EPFL), Geneva, Switzerland

First Author:

Juliette Boscheron  
École polytechnique fédérale de Lausanne (EPFL)
Geneva, Switzerland

Co-Author(s):

Mariana Babo-Rebelo  
École polytechnique fédérale de Lausanne (EPFL)
Geneva, Switzerland
Arthur Trivier  
École polytechnique fédérale de Lausanne (EPFL)
Geneva, Switzerland
Florian Lance  
École polytechnique fédérale de Lausanne (EPFL)
Geneva, Switzerland
Bruno Herbelin  
École polytechnique fédérale de Lausanne (EPFL)
Geneva, Switzerland
Dimitri Van De Ville  
École polytechnique fédérale de Lausanne (EPFL)
Geneva, Switzerland
Olaf Blanke  
École polytechnique fédérale de Lausanne (EPFL)
Geneva, Switzerland

Introduction:

Episodic memory retrieval is often accompanied by autonoetic consciousness (ANC), i.e., a vivid sense of mentally re-experiencing a previously lived event (Tulving, 1972). However, the neural mechanisms underlying such phenomenological experience are still poorly understood. The hippocampus is thought to integrate event-related components into coherent memories and to coordinate cortical activity during retrieval (Barry & Maguire, 2019; Moscovitch et al., 2016), resulting in reinstatement effects in hippocampal (Gilmore et al., 2021; Xue, 2018), visual (Bone et al., 2020; Gordon et al., 2014), and auditory (Gordon et al., 2014; Wheeler et al., 2000) cortical areas. While most research focused on the reinstatement of auditory and visual processes, the participant's body during the encoding of events also provides a rich context of proprioceptive, motor and sensory cues that have only recently been investigated. Recent work has suggested that sense of agency, as well as premotor-hippocampal coupling is involved in the retrieval process (Meyer et al., 2024; Meyer et al., 2024). However, the contribution of motor inputs to ANC is still unknown. Here, we postulated that the motor cortex is reengaged at retrieval through hippocampal-neocortical trace reactivation and that such motor activity participates to ANC.

Methods:

We developed an experimental paradigm in which healthy participants (N=30) encoded new real-life like events requiring motor actions in a 3D highly immersive mixed reality environment. Participants drove a car and encountered obstacles on the road that they removed with a specific movement (2 conditions: Foot and No Foot, requiring different movements). We recorded participants' brain activity while they freely retrieved each of these events in the MRI scanner one day after encoding.
After preprocessing the data with SPM, we computed 1st and 2nd level General Linear Models (GLM) to study the retrieval process. Effects were explored with threshold of p<0.001 cluster-size p-FWE-correction. We also conducted a seed-to-whole brain analysis with the right and left hippocampi as seed regions to quantify the main effect of retrieval using the CONN toolbox (www.nitrc.org/projects/conn). Brain maps were thresholded using Random Field Theory parametric statistics with a threshold of p<0.05 cluster-size p-FWE-corrections.

Results:

Our data show memory related activations in bilateral hippocampus, parahippocampus, angular gyrus, middle temporal gyrus, vmPFC and insula. Critically, we also observe activity in the motor cortex (bilateral primary motor cortex and right SMA) during free retrieval, suggesting that motor cortex is indeed reengaged in the retrieval process (Fig. 1). We additionally observe that activity in supplementary motor area (SMA) and premotor cortex is positively modulated by our participants' intensity of reliving the events, indicating that motor cortex activity plays a significant role in re-experiencing events. We also show that retrieval of events requiring multi-limb movements (Foot events) elicit higher precuneus and angular gyrus activity than simple movements (No Foot events), indicating that motor actions at encoding shape retrieval, engaging body/action-related regions. In a final step, we show that hippocampus to motor cortex functional connectivity is significantly enhanced during free retrieval, suggesting a potential interaction between the hippocampal "memory hub" and motor regions.
Supporting Image: fig1.png
 

Conclusions:

This study provides evidence for action in memory, revealing that the motor context during encoding plays a crucial role in the later retrieval process, during which motor cortex is reengaged and shapes the feeling of re-experiencing events. With increased motor-hippocampal interactions, we also suggest that such motor reengagement could be indexed by hippocampus activity.

Learning and Memory:

Long-Term Memory (Episodic and Semantic) 1

Modeling and Analysis Methods:

Connectivity (eg. functional, effective, structural)
Univariate Modeling 2

Keywords:

Cognition
Consciousness
FUNCTIONAL MRI
Memory
Motor

1|2Indicates the priority used for review

Abstract Information

By submitting your proposal, you grant permission for the Organization for Human Brain Mapping (OHBM) to distribute your work in any format, including video, audio print and electronic text through OHBM OnDemand, social media channels, the OHBM website, or other electronic publications and media.

I accept

The Open Science Special Interest Group (OSSIG) is introducing a reproducibility challenge for OHBM 2025. This new initiative aims to enhance the reproducibility of scientific results and foster collaborations between labs. Teams will consist of a “source” party and a “reproducing” party, and will be evaluated on the success of their replication, the openness of the source work, and additional deliverables. Click here for more information. Propose your OHBM abstract(s) as source work for future OHBM meetings by selecting one of the following options:

I do not want to participate in the reproducibility challenge.

Please indicate below if your study was a "resting state" or "task-activation” study.

Task-activation

Healthy subjects only or patients (note that patient studies may also involve healthy subjects):

Healthy subjects

Was this research conducted in the United States?

No

Were any human subjects research approved by the relevant Institutional Review Board or ethics panel? NOTE: Any human subjects studies without IRB approval will be automatically rejected.

Yes

Were any animal research approved by the relevant IACUC or other animal research panel? NOTE: Any animal studies without IACUC approval will be automatically rejected.

Not applicable

Please indicate which methods were used in your research:

Functional MRI
Structural MRI

For human MRI, what field strength scanner do you use?

3.0T

Which processing packages did you use for your study?

SPM

Provide references using APA citation style.

Barry, D. N. (2019). Remote Memory and the Hippocampus: A Constructive Critique. Trends in Cognitive Sciences, 23(2), 128–142. https://doi.org/10.1016/j.tics.2018.11.005

Bone, M. B. (2020). Feature-specific neural reactivation during episodic memory. Nature Communications, 11(1), 1945. https://doi.org/10.1038/s41467-020-15763-2

Gilmore, A. (2021). Dynamic Content Reactivation Supports Naturalistic Autobiographical Recall in Humans. Journal of Neuroscience, 41(1), 153–166. https://doi.org/10.1523/JNEUROSCI.1490-20.2020

Gordon, A. M. (2014). Cortical Reinstatement Mediates the Relationship Between Content-Specific Encoding Activity and Subsequent Recollection Decisions. Cerebral Cortex, 24(12), 3350–3364. https://doi.org/10.1093/cercor/bht194

Meyer, N. H. (2024). Sense of Agency during Encoding Predicts Subjective Reliving. Eneuro, 11(10), ENEURO.0256-24.2024. https://doi.org/10.1523/ENEURO.0256-24.2024

Meyer, N. H. (2024). Embodiment in episodic memory through premotor-hippocampal coupling. Communications Biology, 7(1), 1111. https://doi.org/10.1038/s42003-024-06757-7

Moscovitch, M. (2016). Episodic Memory and Beyond: The Hippocampus and Neocortex in Transformation. Annual Review of Psychology, 67(1), 105–134. https://doi.org/10.1146/annurev-psych-113011-143733

Tulving, E. (1972). Episodic and Semantic Memory.

Wheeler, M. E. (2000). Memory’s echo: Vivid remembering reactivates sensory-specific cortex. Proceedings of the National Academy of Sciences, 97(20), 11125–11129. https://doi.org/10.1073/pnas.97.20.11125

Xue, G. (2018). The Neural Representations Underlying Human Episodic Memory. Trends in Cognitive Sciences, 22(6), 544–561. https://doi.org/10.1016/j.tics.2018.03.004

UNESCO Institute of Statistics and World Bank Waiver Form

I attest that I currently live, work, or study in a country on the UNESCO Institute of Statistics and World Bank List of Low and Middle Income Countries list provided.

No