Somatotopic replay activity patterns in human motor cortex at rest

Poster No:

1055 

Submission Type:

Abstract Submission 

Authors:

Lorenzo Pini1, Lu Zhang2,1, Gordon Shulman3, Maurizio Corbetta1

Institutions:

1Department of Neuroscience, University of Padova, Padova, Italy, 2The Affiliated Kangning Hospital of Ningbo University, Ningbo , China, 3Departments of Neurology and Radiology, Washington University in Saint Louis, Saint Louis, MO

First Author:

Lorenzo Pini  
Department of Neuroscience, University of Padova
Padova, Italy

Co-Author(s):

Lu Zhang  
The Affiliated Kangning Hospital of Ningbo University|Department of Neuroscience, University of Padova
Ningbo , China|Padova, Italy
Gordon Shulman  
Departments of Neurology and Radiology, Washington University in Saint Louis
Saint Louis, MO
Maurizio Corbetta  
Department of Neuroscience, University of Padova
Padova, Italy

Introduction:

The brain exhibits constant patterns of spontaneous activity, even in the absence of sensory input or tasks. The representation hypothesis (Pezzulo et al., 2021) suggests that spontaneous activity underlies priors of generative models of the most common perceptual, motor, and cognitive patterns, which are used as top-down models to predict future behavior. In line with this hypothesis, in previous work we showed that spontaneous activity patterns in higher visual regions replay category specific patterns in category specific regions (e.g., face patterns in fusiform face area, Kim et al., 2020). Moreover, spontaneous replays of natural hand movements occur in human primary motor cortex and parietal cortex (Livne et al., 2022; Zhang et al., 2023). To further investigate the specificity of motor replay patterns in human motor cortex, we measured the occurrence of motor patterns related to hand, foot, or mouth movements during resting state in somatotopic specific regions along the precentral gyrus. Specifically, whether hand related movement patterns occurred more frequently at rest in the hand region than in the foot or mouth region, and so forth for the other comparisons.

Methods:

Using data from 100 healthy participants (56 females, 22-35 yrs) in the Human Connectome Project (HCP), we analyzed 3T resting-state and task fMRI data. Participants performed hand, foot, and tongue movements based on visual cues. Each 12-second block involved tapping fingers, squeezing toes, or moving the tongue, preceded by a 3-second cue. Each run included 13 blocks: two for tongue, four for hand, four for foot, and three 15-second fixation blocks. A 15-minute resting-state fMRI scan was conducted. Multi-voxel activation patterns in effector-specific regions (ROIs) were measured and compared between preprocessed rest and task surface data. The U90 value (90th percentile of r-value distribution) represented the task-rest pattern similarity and served as the dependent variable in ANOVAs assessing interactions between regions, movements, and hemispheres. We also examined the relationship between U90 values and motor performance (9-hole peg test) using linear and random-forest regression models.

Results:

Results showed a significant three-way interaction between movement patterns, hemisphere, and ROI (F[8,792]=21.73, p<0.001). Task-rest pattern similarity varied by ROI and hemisphere, with hand ROIs resembling finger-tapping patterns and mouth ROIs resembling tongue movements (p<0.001). These findings indicate distinct task-rest spatial similarity patterns in the motor cortex based on movement type, ROI, and hemisphere. This somatotopic specificity was consistent across participants. Additionally, task-rest similarity (U90) positively correlated with activation magnitude for preferred movement patterns (p<0.015) and negatively for non-preferred patterns (p<0.007). No significant relationship emerged between U90 values and motor performance for both the linear and non-linear models (p>0.05).

Conclusions:

We found that resting state multivoxel activity patterns were more like those evoked by the region's preferred movement, supporting the representation hypothesis of spontaneous activity. Spontaneous activity reflects motor synergies and functional tasks commonly performed in daily life. We also observed a positive relationship between activation strength and task-rest similarity for preferred movements, while non-preferred movements showed a negative relationship. This indicates that task-rest similarity depends on functional relevance, not just activation magnitude. No significant relationship was found between task-rest similarity and motor performance, possibly due to ceiling effects in the young healthy cohort. Overall, despite limitations, including a small set of movements, these findings were consistent across subsamples and highlight how resting-state patterns may shape motor cortex organization and development.

Modeling and Analysis Methods:

Activation (eg. BOLD task-fMRI) 1
Task-Independent and Resting-State Analysis

Motor Behavior:

Motor Planning and Execution
Motor Behavior Other 2

Physiology, Metabolism and Neurotransmission:

Neurophysiology of Imaging Signals

Keywords:

Computational Neuroscience
Cortex
FUNCTIONAL MRI
Modeling
MRI
Somatosensory
Systems
Other - cortical replay

1|2Indicates the priority used for review

Abstract Information

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

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Please indicate which methods were used in your research:

Functional MRI
Structural MRI
Neuropsychological testing

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

3.0T

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Provide references using APA citation style.

Livne, T., et al. (2022). Spontaneous activity patterns in human motor cortex replay evoked activity patterns for hand movements. Scientific Reports, 12(1), 16867.

Pezzulo, G., Zorzi, M., & Corbetta, M. (2021). The secret life of predictive brains: What's spontaneous activity for? Trends in Cognitive Sciences, 25(9), 730–743.

Kim, D., Livne, T., Metcalf, N. V., Corbetta, M., & Shulman, G. L. (2020). Spontaneously emerging patterns in human visual cortex and their functional connectivity are linked to the patterns evoked by visual stimuli. Journal of Neurophysiology, 124(5), 1343–1363.

Zhang, L., Pini, L., Kim, D., Shulman, G. L., & Corbetta, M. (2023). Spontaneous activity patterns in human attention networks code for hand movements. Journal of Neuroscience, 43(11), 1976–1986.

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