The hyper-reinnervation of rat skeletal muscle

doi:10.1016/0006-8993(95)00102-V

Brain Research

Volume 676, Issue 1, 3 April 1995, Pages 113-123

https://doi.org/10.1016/0006-8993(95)00102-V Get rights and content

Abstract

This study examines muscle recovery and related changes in the motor unit population of ‘hyper-reinnervated’ rat skeletal muscle. Medial gastrocnemius (MG) muscles were hyper-reinnervated by either cutting the MG nerve and implanting it on the MG muscle together with additional hind limb nerves, or by crushing the MG nerve and excising the medial portion (50–70%) of the MG muscle. Our findings were that muscles hyper-reinnervated with multiple nerves recovered muscle mass and strength more fully than did the self-reinnervated muscles, more motor units were formed (up to three times the normal number were found), and the mean motor unit size was significantly smaller. A relatively small percentage of muscle fibers became polyneuronally innervated. In contrast, the number of motor units that were formed in the muscle reduction experiments were not significantly larger than was expected considering the mass of the muscles. We conclude that hyper-reinnervation improves muscle recovery, it may be a useful technique for improving function in denervated muscle, and may serve to provide added sources of EMG control signals in some amputees.

References (21)

OstbergA.J. et al.
Reinnervation of fast and slow mammalian muscles by a superfluous number of motor axons
Neuroscience
(1986)
PeyronnardJ.M. et al.
Motor, sympathetic and sensory innervation of rat skeletal muscles
Brain Res.
(1986)
AbercrombieM.
Estimation of nuclear population from microtome sections
Anat. Rec.
(1946)
BungeR.P.
Some observations on the role of the schwann cell in peripheral nerve regeneration
FrankE. et al.
Maintained function of foreign synapses on hyperinnervated skeletal muscle fibres of the rat
Nature
(1974)
FreyM. et al.
An experimental comparison of the different kinds of muscle reinnervation: nerve suture, nerve implantation, and muscular neurotization
Plast. Reconstr. Surg.
(1982)
GillespieM.J. et al.
Reinnervation of the lateral gastrocnemius and soleus muscles in the rat by their common nerve
J. Physiol.
(1986)
GillespieM.J. et al.
Motor unit and histochemistry in rat lateral gastrocnemius and soleus muscles: evidence for dissociation of physiological and histochemical properties after reinnervation
J. Neurophysiol.
(1987)
GordonT. et al.
Time course and extent of recovery in reinnervated motor units of cat triceps surae muscles
J. Physiol.
(1982)
HashizumeK. et al.
Medial gastrocnemius motor nucleus in the rat: age-related changes in the number and size of motoneurons
J. Comp. Neurol.
(1988)

There are more references available in the full text version of this article.

Cited by (68)

Rehabilitation of high upper limb amputees after Targeted Muscle Reinnervation
2022, Journal of Hand Therapy
Citation Excerpt :
Targeted muscle reinnervation (TMR) is a surgical technique of selective nerve transfers to provide patients suffering from high upper limb amputations with up to six myoelectric signals for intuitive prosthetic control.1,2 During surgery, blindly ending residual nerves, which formerly controlled elbow and hand function, are transferred to specific muscles of the residual limb and trunk that are no longer of functional use.3,4 After nerve regeneration and a period of intense cognitive motor training, the reinnervated muscles serve as biological amplifiers for the neural command to the prosthetic arm.
This is a Delphi study based on a scoping literature review.
Targeted muscle reinnervation (TMR) enables patients with high upper limb amputations to intuitively control a prosthetic arm with up to six independent control signals. Although there is a broad agreement regarding the importance of structured motor learning and prosthetic training after such nerve transfers, to date, no evidence-based protocol for rehabilitation after TMR exists.
We aimed at developing a structured rehabilitation protocol after TMR surgery after major upper limb amputation. The purpose of the protocol is to guide clinicians through the full rehabilitation process, from presurgical patient education to functional prosthetic training.
European clinicians and researchers working in upper limb prosthetic rehabilitation were invited to contribute to a web-based Delphi study. Within the first round, clinical experts were presented a summary of recent literature and were asked to describe the rehabilitation steps based on their own experience and scientific evidence. The second round was used to refine these steps, while the importance of each step was rated within the third round.
Experts agreed on a rehabilitation protocol that consists of 16 steps and starts before surgery. It is based on two overarching principles, namely the necessity of multiprofessional teamwork and a careful selection and education of patients within the rehabilitation team. Among the different steps in therapy, experts rated the training with electromyographic biofeedback as the most important one.
Within this study, a first rehabilitation protocol for TMR patients based on a broad experts' consensus and relevant literature could be developed. The detailed steps for rehabilitation start well before surgery and prosthetic fitting, and include relatively novel interventions as motor imagery and biofeedback. Future studies need to further investigate the clinical outcomes and thereby improve therapists’ practice.
Graded rehabilitation offered by a multiprofessional team is needed to enable individuals with upper limb amputations and TMR to fully benefit from prosthetic reconstruction.
Low.
Targeted Muscle Reinnervation for Prosthetic Control
2021, Hand Clinics
Citation Excerpt :
Furthermore, most nerve transfers used in TMR are multifascicular nerves that usually innervate multiple nerves and instead are rerouted to single target muscles. This leads to hyper-reinnervation of the targeted muscle with smaller individually controllable motor units.27–29 This surplus of potential axons for reinnervation and the short axonal regeneration distances for reinnervation are likely the reason for the high success rate of this procedure in terms of reinnervation.
Targeted reinnervation for somatosensory feedback
2021, Somatosensory Feedback for Neuroprosthetics
Targeted reinnervation was introduced as a surgical procedure to improve myoelectric control signals for proximal upper limb amputation. From the first case studies in patients with shoulder disarticulation and transhumeral amputation, it was noted that in addition to increased motor control signals, there was restoration of sensations related to the missing arm and hand. The neural remapping of hand sensation has been explored as an avenue for tactile feedback related to the cutaneous reinnervation, and kinesthetic feedback related to the reinnervation of the muscle sensory fibers. Advances in robotic haptic devices and prosthesis sensorization have led to fully integrated wearable prosthesis systems that noninvasively provide real-time somatotopically and modality-matched feedback. These bidirectional neural human–machine interface systems provide insight into the underlying neural mechanisms of sensory processing and integration. Planning for targeted reinnervation should include a thorough assessment of potential motor sites, nerve management, and sensory restoration options.
Targeted Muscle Reinnervation and the Volar Forearm Filet Flap for Forequarter Amputation: Description of Operative Technique
2020, Journal of Hand Surgery Global Online
Citation Excerpt :
After forequarter amputation, the resection typically extends through the clavicle, and the brachial plexus is truncated at the level of the trunks or divisions, which then serve as the donor nerves for reinnervation into the more peripheral radial, ulnar, and median nerves of the free flap. A size mismatch is expected, but the large brachial plexus trunks provide hyperinnervation, which promotes target muscle reinnervation.16 The patient is placed in the lateral decubitus position with the arm prepared for surgery and free to allow for manipulation during the forequarter amputation.
Targeted muscle reinnervation after upper-extremity amputation has demonstrated improved outcomes with myoelectric prosthesis function and postoperative neuropathic pain. This technique has been established in the setting of shoulder disarticulation as well as transhumeral and transradial amputations, but a detailed technique of targeted muscle reinnervation with free tissue transfer from the volar forearm after forequarter amputation has not yet been described. Here, we describe a technique using a volar forearm filet flap to achieve simultaneously satisfactory soft tissue coverage after resection of a tumor from the chest wall and targeted muscle reinnervation of the brachial plexus.
Pedicled Serratus Anterior Flap as an Alternative Muscle Target for Targeted Muscle Reinnervation in Transhumeral Amputees
2019, Journal of Hand Surgery
Upper limb amputation is a universally devastating injury that results in substantial loss of function. Myoelectric prostheses represent a new generation of battery-powered programmable prostheses controlled by EMG signals. The aim of upper limb targeted muscle reinnervation (TMR) is to enhance the control of a myoelectric prosthesis by improving the number and quality of EMG signals that can be used to control prosthetic elbow, wrist, and hand movements. Current TMR techniques rely on preservation of parts of biceps and triceps to be used as reinnervated muscle targets. However, a subset of amputations exists in which the proximity or mechanism of injury results in loss of these local muscle targets, making these techniques less suitable. Alternative muscles beyond the zone of injury must be sought and imported as targets for residual nerves. Through its neurovascular anatomy and physical structure, the serratus anterior offers multiple potential targets in close vicinity to the upper limb, making the creation of additional signals through a single flap achievable in this challenging scenario. We present our technique using a pedicled serratus anterior muscle flap as an alternative muscle target in transhumeral amputees undergoing TMR.
Upper-limb prosthetic devices
2018, Handbook of Biomechatronics
Upper-limb prosthetic devices demand high performance technology to work hand in hand with human body for replacing one of the most delicate “tools” of nature, the human hand. In this chapter, we try to highlight the foundational elements, advancements and challenges for moving to high performance control of many-degrees-of-freedom upper-limb prostheses. As expected, the advances span across many different areas of engineering (robotics, sensors, control, and nanotechnology), biology, and medicine.

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The hyper-reinnervation of rat skeletal muscle

Abstract

Neuroscience

Brain Res.

Estimation of nuclear population from microtome sections

Anat. Rec.

Some observations on the role of the schwann cell in peripheral nerve regeneration

Maintained function of foreign synapses on hyperinnervated skeletal muscle fibres of the rat

Nature

An experimental comparison of the different kinds of muscle reinnervation: nerve suture, nerve implantation, and muscular neurotization

Plast. Reconstr. Surg.

Reinnervation of the lateral gastrocnemius and soleus muscles in the rat by their common nerve

J. Physiol.

Motor unit and histochemistry in rat lateral gastrocnemius and soleus muscles: evidence for dissociation of physiological and histochemical properties after reinnervation

J. Neurophysiol.

Time course and extent of recovery in reinnervated motor units of cat triceps surae muscles

J. Physiol.

Medial gastrocnemius motor nucleus in the rat: age-related changes in the number and size of motoneurons

J. Comp. Neurol.