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How natural hand usage shapes behavior and intrinsic and task-evoked brain activity.

Periodic Reporting for period 4 - HANDmade (How natural hand usage shapes behavior and intrinsic and task-evoked brain activity.)

Période du rapport: 2022-08-01 au 2024-01-31

Evidence indicates that the brain's functional organization is not primarily dependent upon stimulus-related processing. Instead, the cognitive operations of the brain appear mainly intrinsic. For many years, the brain has been explored in terms of task-induced increases of regional brain activity (i.e. activation) during goal-directed behaviors compared to a state of control. More recently, the state of control has become a window to study the brain's functional organization. The major focus of this project is to explain how the intrinsic activity of the brain relates to psychological functions and behavior.

This framework not only has great implications for developmental and experimental psychology, but also for educational training programs and for robotic-assisted technology. Understanding which resources are used by the brain for controlling tools in natural settings is crucial for the future development of biomedical technology that uses robotic systems to perform new and more precise operations possible (as those implemented in micro-surgery). Over time, this technology could make its entrance into industry, e.g. in the field of precision assembly, with positive effects on the physical burden of the workers. Finally, better knowledge of the physiological phenomena underlying the neuroprostheses' control capability might greatly impact the training procedure that amputees undergo to control the prosthesis.

This project tests the hypothesis that the intrinsic brain represents and maintains an internal model of the body form and common movements performed by the hand. The working model of this project posits that this internal activity serves as a model that constrains a functional structure through physical interaction with the surroundings, with the hand playing a crucial role as the primary means of interaction. The second objective is to assess the resilience of this model to extreme body manipulations. This multidisciplinary project tackles fundamental questions in psychology and neuroscience. Ultimately, this grant could pave the way for new applications in robotic-assisted technology, such as those used in micro-surgery and neuroprostheses.

CONCLUSIONS OF THE ACTION
We mapped multivariate spatiotemporal patterns of activity and connectivity associated with natural hand movements and behaviors in the intrinsic activity. To do this, we employed fMRI to examine the spatial patterns and MEG to analyze the temporal patterns at a high temporal resolution. Additionally, we conducted a study to test whether intrinsic activity maintains a model of the body concomitantly using high-density EEG and hand kinematics in naturalistic settings. Then, we tested the resilience of this internal model by examining the modification of the tight relationship between behavior and the effector we use to interact with the external environment. We investigated the embodiment of a virtual bionic tool and a virtual hand in healthy participants and showed that the virtual grafting of a bionic tool elicits a sense of embodiment similar to or even stronger than its natural counterpart. Overall, the natural usage of bionic tools can rewire the evolution of human behavior.
We tested whether spontaneous activity in the human somatomotor cortex is modulated by visual stimuli that display hands vs. non-hand stimuli and by the use/action they represent. In the left somatomotor cortex, we observed a stronger (multivoxel) spatial correlation between resting-state activity and natural hand picture patterns compared to other stimuli. We conclude that spontaneous activity patterns in somatomotor brain regions code for the visual representation of human hands and their use. This study is under review (El Rassi et al., Scientific Reports). In a second fMRI study in preparation (Perciballi et al.,), we showed that mere observation of everyday hand gestures are highly represented in spontaneous activity patterns across the association cortex as compared to those evoked by uncommon hand grasps. Same sample and paradigms were used to conduct an high-density EEG study (in preparation). These findings suggest that statistical regularities of the hand movement resonate in spontaneous activity. In a third study in preparation (Ramundo et al., ) we investigated the brain mechanisms of distinguishing between one's own and others' movements in the absence of aesthetic or morphological features. This is a preliminary step to understand whether the recognition of their own gesture is already encoded in the spontaneous activity. Intransitive actions were significantly more recognizable than transitive ones. fMRI results confirmed dissociable neural correlates of observing intransitive versus transitive actions. Our results show that the idiosyncrasies in the kinematics of self-generated actions, fundamental for the recognition of one’s own gesture, elicit the activation of action-related structures that participate in the distinction self/other.

In a MEG study, we tested whether hand dexterity is already encoded in spontaneous activity. Results have already been published in the peer-reviewed and high-impact factor The Journal of Neuroscience (Maddaluno et al., 2024). By using kinematics, we performed a characterization of the hand states and dynamics occurring in participants throughout an ecological setting. Results of this finding have been published in the peer-reviewed and high-impact factor journal, Scientific Reports (Sili et al., 2023). Based on this study, we are now studying whether the spatiotemporal architecture of manual behavior is already encoded in the spontaneous activity, by performing an high-density EEG study. We firstly conducted a methodological study to define the regularization parameter for estimating the functional connectivity during resting-state. Results of this finding are in revision (Neuroimage).

Using an implicit measure of embodiment and a motor task, across four experiments, we consistently show that the virtual grafting of a bionic tool elicits a sense of embodiment similar to or even stronger than its natural counterpart. This study has been accepted for publication in iScience (Marucci-Maddaluno et al., 2024). A similar paradigm was also employed in upper-limb amputees, using a 4-weeks long training using virtual reality. Before and after it, participants performed a fMRI study to study the functional brain organization, studied using measures of brain activity, connectivity, graph analysis, during resting-state and task-evoked activity. Results of these experiments were in preparation.
We showed that the hand, in terms of form, common gestures, dynamics of the movements and dexterity, is already encoded in spontaneous activity. Unexpectedly, we also showed that a virtual bionic tool elicits a sense of embodiment similar to or even stronger than a virtual hand and the motor performance is even higher. Application of this paradigm in upper-limb amputation during a 4 weeks training will also allow study also the brain reorganization using fMRI.
We realized that a similar paradigm could be applied to the rehabilitation of amputated limbs. Thus, we developed an integrated platform, using virtual reality and electromyography (EMG) for the real-time classification of movements in the residual limb. This drive towards innovation and applied research conducted my research team to be granted by proof-of-concept (POC) call.
results by Maddaluno et al. Journal of Neuroscience, 2024
results by Marucci-Maddaluno et al.,, iScience 2024
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