Principles of human movement augmentation and the challenges in making it a reality

Eden, Jonathan; Bräcklein, Mario; Ibáñez, Jaime; Barsakcioglu, Deren Y.; Pino, Giovanni Di; Farina, Dario; Burdet, Etienne; Mehring, Carsten

doi:10.1038/s41467-022-28725-7

Cited by 65 publications

(46 citation statements)

References 119 publications

(222 reference statements)

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“…We showed that by closing the loop with a peripheral neural interface based on MU activity, subjects could volitionally modulate the power of cortical β bursts. This could provide new possibilities to exploit cortical β, for example, as a control signal for virtual or robotic effectors ( Dominijanni et al, 2021 ; Eden et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

Reading and Modulating Cortical β Bursts from Motor Unit Spiking Activity

et al. 2022

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β Oscillations (13–30 Hz) are ubiquitous in the human motor nervous system. Yet, their origins and roles are unknown. Traditionally, β activity has been treated as a stationary signal. However, recent studies observed that cortical β occurs in “bursting events,” which are transmitted to muscles. This short-lived nature of β events makes it possible to study the main mechanism of β activity found in the muscles in relation to cortical β. Here, we assessed whether muscle β activity mainly results from cortical projections. We ran two experiments in healthy humans of both sexes ( N = 15 and N = 13, respectively) to characterize β activity at the cortical and motor unit (MU) levels during isometric contractions of the tibialis anterior muscle. We found that β rhythms observed at the cortical and MU levels are indeed in bursts. These bursts appeared to be time-locked and had comparable average durations (40–80 ms) and rates (approximately three to four bursts per second). To further confirm that cortical and MU β have the same source, we used a novel operant conditioning framework to allow subjects to volitionally modulate MU β. We showed that volitional modulation of β activity at the MU level was possible with minimal subject learning and was paralleled by similar changes in cortical β activity. These results support the hypothesis that MU β mainly results from cortical projections. Moreover, they demonstrate the possibility to decode cortical β activity from MU recordings, with a potential translation to future neural interfaces that use peripheral information to identify and modulate activity in the central nervous system. SIGNIFICANCE STATEMENT We show for the first time that β activity in motor unit (MU) populations occurs in bursting events. These bursts observed in the output of the spinal cord appear to be time-locked and share similar characteristics of β activity at the cortical level, such as the duration and rate at which they occur. Moreover, when subjects were exposed to a novel operant conditioning paradigm and modulated MU β activity, cortical β activity changed in a similar way as peripheral β. These results provide evidence for a strong correspondence between cortical and peripheral β activity, demonstrating the cortical origin of peripheral β and opening the pathway for a new generation of neural interfaces.

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Section: Discussionmentioning

confidence: 99%

Reading and Modulating Cortical β Bursts from Motor Unit Spiking Activity

et al. 2022

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“…Possible extracted control signals may depend on behavioural changes and not on a designated descending control command, and therefore, may not satisfy the intended application. Similar constraints effectively apply for augmentation when the aim is to extend the degrees of freedom that a human can volitional control, that is, adding supernumerary degrees of freedom to the natural ones ( Eden et al, 2022 ; Dominijanni et al, 2021 ). In such cases, if the control of a supernumerary degree of freedom is based on single MU activation, this activation must be uncoupled from motor behaviour to ensure coordination between natural and supernumerary effectors.…”

Section: Discussionmentioning

confidence: 99%

“…This would correspond to breaking common input into multiple inputs. Nevertheless, even based on behavioural changes, single MU control can be a resource for specific neural-interface applications, for example, in the absence of any additional motor information or to augment a specific motor task (see Eden et al, 2022 for augmentation by transfer ).…”

Section: Discussionmentioning

confidence: 99%

“…If single MUs could be individually controlled, they could potentially be activated in a multitude of ways, leading to an enormous potential for additional information transfer. New MU activation patterns made of independent control of units could then be used to provide the basis for augmented control signals without impeding the original function of the innervated muscles for natural limb control ( Eden et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

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The control and training of single motor units in isometric tasks are constrained by a common input signal

Bräcklein

Barsakcioglu

Ibáñez

et al. 2022

eLife

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Recent developments in neural interfaces enable the real-time and non-invasive tracking of motor neuron spiking activity. Such novel interfaces could provide a promising basis for human motor augmentation by extracting potentially high-dimensional control signals directly from the human nervous system. However, it is unclear how flexibly humans can control the activity of individual motor neurons to effectively increase the number of degrees-of-freedom available to coordinate multiple effectors simultaneously. Here, we provided human subjects (N=7) with real-time feedback on the discharge patterns of pairs of motor units (MUs) innervating a single muscle (tibialis anterior) and encouraged them to independently control the MUs by tracking targets in a 2D space. Subjects learned control strategies to achieve the target-tracking task for various combinations of MUs. These strategies rarely corresponded to a volitional control of independent input signals to individual MUs during the onset of neural activity. Conversely, MU activation was consistent with a common input to the MU pair, while individual activation of the MUs in the pair was predominantly achieved by alterations in de-recruitment order that could be explained with history-dependent changes in motor neuron excitability. These results suggest that flexible MU recruitment based on independent synaptic inputs to single MUs is unlikely, although de-recruitment might reflect varying inputs or modulations in the neuron's intrinsic excitability.

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“…We are interested in the idea of minimizing physical disabilities of users in the virtual worlds through specially designed virtual avatars 38 . Human movement augmentation such as supernumerary limbs, body-parts remapping, and exoskeletons expands physical abilities both for impaired and unimpaired individuals 39 – 42 . Virtual co-embodiments like the shared body 7 , 8 and our joint body could expand human collaborations as a co-embodied avatar by combining different persons’ strengths and compensating weaknesses.…”

Section: Discussionmentioning

confidence: 99%

Knowing the intention behind limb movements of a partner increases embodiment towards the limb of joint avatar

Hapuarachchi

Kitazaki

2022

Sci Rep

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We explored a concept called “virtual co-embodiment”, which enables users to share their virtual avatars with others. Co-embodiment of avatars and robots can be applied for collaboratively performing complicated tasks, skill training, rehabilitation, and aiding disabled users. We conducted an experiment where two users could co-embody one “joint avatar” in first person view and control different arms to collaboratively perform three types of reaching tasks. We measured their senses of agency and ownership towards the two arms of the avatar and changes in skin conductance levels in response to visual stimuli threatening the two virtual arms. We found that sense of agency, ownership, and skin conductance were significantly higher towards the virtual arm with control compared to the arm controlled by the partner. Furthermore, the senses of agency and ownership towards the arm controlled by the partner were significantly higher when the participant dyads shared a common intention or when they were allowed to see their partner’s target, compared to when the partner’s target was invisible. These results show that while embodiment towards partner-controlled limbs is lower compared to limbs with control, visual information necessary for predicting the partner’s intentions can significantly enhance embodiment towards partner-controlled limbs during virtual co-embodiment.

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Principles of human movement augmentation and the challenges in making it a reality

Cited by 65 publications

References 119 publications

Reading and Modulating Cortical β Bursts from Motor Unit Spiking Activity

Reading and Modulating Cortical β Bursts from Motor Unit Spiking Activity

The control and training of single motor units in isometric tasks are constrained by a common input signal

Knowing the intention behind limb movements of a partner increases embodiment towards the limb of joint avatar

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