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fMRI Confirms Agonist–Antagonist Myoneural Interface Amputation Improves Motor Execution, Sensory Perception

Key findings

  • A new amputation procedure, agonist–antagonist myoneural interface amputation (AA), is designed to allow proprioceptive signals from preserved muscles to be communicated to the central nervous system
  • During functional MRI scanning, central sensorimotor mechanisms were evaluated in 12 subjects who had undergone AA, 10 who had undergone traditional amputation (TA) and 10 who had not undergone amputation (NA)
  • The part of the brain that received proprioceptive input was activated similarly in the AA and NA groups, but the TA group demonstrated decreased activation
  • Performance on tasks requiring motor control and proprioception was better in the AA group than the TA group
  • AA should be regarded not as a failure of limb salvage but rather as a form of reconstructive surgery where sensory feedback can be preserved

Traditional amputation substantially disrupts the normal sensorimotor mechanisms of the central nervous system. One major problem is that agonist–antagonist muscle pairs—which signal force, velocity and position to the brain—are severed, interfering with proprioception (sensory feedback).

A new procedure, agonist–antagonist myoneural interface (AMI) amputation, uses muscle grafts from the patient's body and existing nerves at a lower limb amputation site to create muscle pairs that mimic those found in uninjured limbs. An agonist and an antagonist muscle are surgically connected in series within the residual limb, with the expectation that mechanoreceptors within both muscles will communicate proprioceptive information to the central nervous system and vice versa.

Shriya S. Srinivasan, PhD, postdoc, Samantha Gutiérrez-Arango, senior research support associate, PhD student Hyun-Geun Song, and Robert L. Barry, PhD, assistant physicist, of the Martinos Center for Biomedical Imaging at Massachusetts General Hospital; Hugh Herr, PhD, of the MIT Center for Extreme Bionics; and colleagues recently provided the first direct evidence that AMI amputation can preserve central sensorimotor mechanisms, giving patients a better chance to control an advanced neuroprosthesis. Their report appears in Science Translational Medicine.

Study Methods

The study participants were:

  • 12 subjects who had undergone unilateral trans-tibial AMI amputation (AA)
  • 7 subjects who had undergone traditional amputation (TA), matched to the AA group on age and time since amputation
  • 10 subjects who had not undergone amputation (NA)

The TA and AA groups had similar rehabilitation and gait training, and all subjects in those groups were currently using a passive prosthesis regularly. All subjects underwent functional MRI while the researchers led them through tests of motor execution and sensory perception.

Fascicle Dynamics

Proprioception input to the brain is received in Brodmann area (BA) 3a. During neuroimaging, when subjects flexed their ankle or phantom ankle, BA3a was activated to a similar extent in the AA and NA groups. Activation was significantly less in the TA group than the NA group.

Motor Control

Subjects were then asked to move their ankle or phantom ankle to specific locations, a test of proprioception, motor control and neuroprosthetic controllability. Performance, evaluated using electromyographic signals from AMI muscles, correlated linearly with activation of BA3a and was significantly better in the AA group than in the TA group.

Phantom Sensation

The researchers analyzed functional connectivity as the subjects were at rest or performing a task. During the resting state, most individuals in the AA group had phantom sensation scores greater than 6/10 and demonstrated lower connectivity of the visual and sensorimotor networks than those in the TA group.

Clinical Outlook

After TA, people generally rely heavily on their vision to guide their prosthetic limb. The functional connectivity findings suggest AA may reduce patients' dependence on their vision. In addition, previous studies have indicated that greater phantom sensation actually improves motor control and provides a sense of agency.

In all, it seems that AA can "rewire" peripheral neural substrates so that sensory feedback and motor capabilities are restored to pre-amputation levels. AA should be regarded not as a failure of limb salvage but rather as a form of reconstructive surgery.

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