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Agonist-antagonist myoneural interface amputation preserves proprioceptive sensorimotor neurophysiology in lower limbs.

ABSTRACT: The brain undergoes marked changes in function and functional connectivity after limb amputation. The agonist-antagonist myoneural interface (AMI) amputation is a procedure that restores physiological agonist-antagonist muscle relationships responsible for proprioceptive sensory feedback to enable greater motor control. We compared results from the functional neuroimaging of individuals (n = 29) with AMI amputation, traditional amputation, and no amputation. Individuals with traditional amputation demonstrated a significant decrease in proprioceptive activity, measured by activation of Brodmann area 3a, whereas functional activation in individuals with AMIs was not significantly different from controls with no amputation (P < 0.05). The degree of proprioceptive activity in the brain strongly correlated with fascicle activity in the peripheral muscles and performance on motor tasks (P < 0.05), supporting the mechanistic basis of the AMI procedure. These results suggest that surgical techniques designed to restore proprioceptive peripheral neuromuscular constructs result in desirable central sensorimotor plasticity.

SUBMITTER: Srinivasan SS

PROVIDER: S-EPMC7786239 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Agonist-antagonist myoneural interface amputation preserves proprioceptive sensorimotor neurophysiology in lower limbs.

Srinivasan Shriya S SS Tuckute Greta G Zou Jasmine J Gutierrez-Arango Samantha S Song Hyungeun H Barry Robert L RL Herr Hugh M HM

Science translational medicine 20201201 573

The brain undergoes marked changes in function and functional connectivity after limb amputation. The agonist-antagonist myoneural interface (AMI) amputation is a procedure that restores physiological agonist-antagonist muscle relationships responsible for proprioceptive sensory feedback to enable greater motor control. We compared results from the functional neuroimaging of individuals (<i>n</i> = 29) with AMI amputation, traditional amputation, and no amputation. Individuals with traditional a ...[more]

PMID: 33298564

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Project description:The agonist-antagonist myoneural interface (AMI), a surgical method to reinnervate physiologically-relevant proprioceptive feedback for control of limb prostheses, has demonstrated the ability to provide natural afferent sensations for limb amputees when actuating their prostheses. Following AMI surgery, one potential challenge is atrophy of the disused muscles, which would weaken the reinnervation efficacy of AMI. It is well known that electrical muscle stimulus (EMS) can reduce muscle atrophy. In this study, we conducted an animal investigation to explore whether the EMS can significantly improve the electrophysiological performance of AMI. AMI surgery was performed in 14 rats, in which the distal tendons of bilateral solei donors were connected and positioned on the surface of the left biceps femoris. Subsequently, the left tibial nerve and the common peroneus nerve were sutured onto the ends of the connected donor solei. Two stimulation electrodes were affixed onto the ends of the donor solei for EMS delivery. The AMI rats were randomly divided into two groups. One group received the EMS treatment (designated as EMS_on) regularly for eight weeks and another received no EMS (designated as EMS_off). Two physiological parameters, nerve conduction velocity (NCV) and motor unit number, were derived from the electrically evoked compound action potential (CAP) signals to assess the electrophysiological performance of AMI. Our experimental results demonstrated that the reinnervated muscles of the EMS_on group generated higher CAP signals in comparison to the EMS_off group. Both NCV and motor unit number were significantly elevated in the EMS_on group. Moreover, the EMS_on group displayed statistically higher CAP signals on the indirectly activated proprioceptive afferents than the EMS_off group. These findings suggested that EMS treatment would be promising in enhancing the electrophysiological performance and facilitating the reinnervation process of AMI.

Project description:BackgroundNeuroprosthetic devices controlled by persons with standard limb amputation often lack the dexterity of the physiological limb due to limitations of both the user's ability to output accurate control signals and the control system's ability to formulate dynamic trajectories from those signals. To restore full limb functionality to persons with amputation, it is necessary to first deduce and quantify the motor performance of the missing limbs, then meet these performance requirements through direct, volitional control of neuroprosthetic devices.MethodsWe develop a neuromuscular modeling and optimization paradigm for the agonist-antagonist myoneural interface, a novel tissue architecture and neural interface for the control of myoelectric prostheses, that enables it to generate virtual joint trajectories coordinated with an intact biological joint at full physiologically-relevant movement bandwidth. In this investigation, a baseline of performance is first established in a population of non-amputee control subjects ([Formula: see text]). Then, a neuromuscular modeling and optimization technique is advanced that allows unilateral AMI amputation subjects ([Formula: see text]) and standard amputation subjects ([Formula: see text]) to generate virtual subtalar prosthetic joint kinematics using measured surface electromyography (sEMG) signals generated by musculature within the affected leg residuum.ResultsUsing their optimized neuromuscular subtalar models under blindfolded conditions with only proprioceptive feedback, AMI amputation subjects demonstrate bilateral subtalar coordination accuracy not significantly different from that of the non-amputee control group (Kolmogorov-Smirnov test, [Formula: see text]) while standard amputation subjects demonstrate significantly poorer performance (Kolmogorov-Smirnov test, [Formula: see text]).ConclusionsThese results suggest that the absence of an intact biological joint does not necessarily remove the ability to produce neurophysical signals with sufficient information to reconstruct physiological movements. Further, the seamless manner in which virtual and intact biological joints are shown to coordinate reinforces the theory that desired movement trajectories are mentally formulated in an abstract task space which does not depend on physical limb configurations.

Project description:BackgroundFollowing an amputation, the human postural control system develops neuromuscular adaptations to regain an effective postural control. We investigated the compensatory mechanisms behind these adaptations and how sensorimotor integration is affected after a lower-limb transfemoral amputation.MethodsCenter of pressure (CoP) data of 12 unilateral transfemoral amputees and 12 age-matched able-bodied subjects were recorded during quiet standing with eyes open (EO) and closed (EC). CoP adjustments under each leg were recorded to study their contribution to posture control. The spatial structure of the CoP displacements was characterized by measuring the mean distance, the mean velocity of the CoP adjustments, and the sway area. The Entropic Half-Life (EnHL) quantifies the temporal structure of the CoP adjustments and was used to infer disrupted sensory feedback loops in amputees. We expanded the analysis with measures of weight-bearing imbalance and asymmetry, and with two standardized balance assessments, the Berg Balance Scale (BBS) and Timed Up-and-Go (TUG).ResultsThere was no difference in the EnHL values of amputees and controls when combining the contributions of both limbs (p = 0.754). However, amputees presented significant differences between the EnHL values of the intact and prosthetic limb (p < 0.001). Suppressing vision reduced the EnHL values of the intact (p = 0.001) and both legs (p = 0.028), but not in controls. Vision feedback in amputees also had a significant effect (increase) on the mean CoP distance (p < 0.001), CoP velocity (p < 0.001) and sway area (p = 0.007). Amputees presented an asymmetrical stance. The EnHL values of the intact limb in amputees were positively correlated to the BBS scores (EO: ρ = 0.43, EC: ρ = 0.44) and negatively correlated to the TUG times (EO: ρ = - 0.59, EC: ρ = - 0.69).ConclusionThese results suggest that besides the asymmetry in load distribution, there exist neuromuscular adaptations after an amputation, possibly related to the loss of sensory feedback and an altered sensorimotor integration. The EnHL values suggest that the somatosensory system predominates in the control of the intact leg. Further, suppressing the visual system caused instability in amputees, but had a minimal impact on the CoP dynamics of controls. These findings points toward the importance of providing somatosensory feedback in lower-limb prosthesis to reestablish a normal postural control.Trial registrationDRKS00015254 , registered on September 20th, 2018.

Project description:Brain-computer interfaces (BCI) can be designed with several feedback modalities. To promote appropriate brain plasticity in therapeutic applications, the feedback should guide the user to elicit the desired brain activity and preferably be similar to the imagined action. In this study, we employed magnetoencephalography (MEG) to measure neurophysiological changes in healthy subjects performing motor imagery (MI) -based BCI training with two different feedback modalities. The MI-BCI task used in this study lasted 40-60 min and involved imagery of right- or left-hand movements. 8 subjects performed the task with visual and 14 subjects with proprioceptive feedback. We analysed power changes across the session at multiple frequencies in the range of 4-40 Hz with a generalized linear model to find those frequencies at which the power increased significantly during training. In addition, the power increase was analysed for each gradiometer, separately for alpha (8-13 Hz), beta (14-30 Hz) and gamma (30-40 Hz) bands, to find channels showing significant linear power increase over the session. These analyses were applied during three different conditions: rest, preparation, and MI. Visual feedback enhanced the amplitude of mainly high beta and gamma bands (24-40 Hz) in all conditions in occipital and left temporal channels. During proprioceptive feedback, in contrast, power increased mainly in alpha and beta bands. The alpha-band enhancement was found in multiple parietal, occipital, and temporal channels in all conditions, whereas the beta-band increase occurred during rest and preparation mainly in the parieto-occipital region and during MI in the parietal channels above hand motor regions. Our results show that BCI training with proprioceptive feedback increases the power of sensorimotor rhythms in the motor cortex, whereas visual feedback causes mainly a gamma-band increase in the visual cortex. MI-BCIs should involve proprioceptive feedback to facilitate plasticity in the motor cortex.

Dataset Information

Agonist-antagonist myoneural interface amputation preserves proprioceptive sensorimotor neurophysiology in lower limbs.

Publications

Agonist-antagonist myoneural interface amputation preserves proprioceptive sensorimotor neurophysiology in lower limbs.

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