Muscles autotransplantation is an important way to restore motor activity in case
of injury or diseases associated with a loss of muscles ability. One of the typical
examples of such pathology is arthrogryposis multiplex congenita (AMC). Arthrogryposis
is one of the most serious congenital malformations of the musculoskeletal system.
It is characterized by the presence of two or more major joint contractures, muscle
damage, and motoneuronal dysfunction in the anterior horns of the spinal cord. One
of the main problems that determines the limitation or even impossibility of self-care
of patients suffering from arthrogryposis is the lack of active movements in the upper
limb joints, which can be restored by autotransplantation of the muscles of various
donor areas (Hall, 1997; Bamshad et al., 2009; Loeffler and Lewis, 2016).
A major limiting factor for the adequate self-care in patients with this pathology
is a lack of the active elbow flexion due to the fibro-fatty degeneration of the flexors
of the forearm. Such deficits significantly affect the quality of life because many
vital functions are associated with the elbow movements, for example, bringing food
to the mouth. Thus, for these patients it is important to secure functional recovery
of the biceps brachii muscle, which is performed by non-free (with preservation of
the vascular-muscular bundle) autotransplantation of the muscles surrounding the shoulder
joint (commonly by the pectoralis major or the latissimus dorsi muscles) (Oishi et
al., 2017). The loss of the muscle function in the donor region does not cause any
significant functional impairment due to the work of the remaining synergistic muscles
(Mikati, 2007; Zargarbashi et al., 2017).
There are two pivotal and non-trivial aspects witch should be addressed for such surgeries:
Which muscle is the most suitable for the autotransplantation?
How to facilitate the rehabilitation processes after the muscle autotransplantation?
Next, we discuss these two issues in more detail.
Which Muscle is the Most Suitable for the Autotransplantation?
At the first consideration of such a question, the most important criteria may be
the anatomical, biomechanical, biochemical compatibility of the transplanted muscle
to the original one (Hoang et al., 2018) and the peculiarities of their representations
at the central nervous system level. The current criteria for choosing a donor muscle
are: muscle strength of at least 3 points on a 5-point scale (MRC Scale for Muscle
Strength) and the minimal damage to the donor area.
In this opinion we would like to focus primarily on the processes associated with
the cortical muscles representations. Upper limb is used mainly to perform voluntary
movements (unlike lower limbs whose most crucial function is locomotion), thus the
cortical level plays here a crucial role (Pettersson et al., 2007; Lemon, 2008). The
most studied question in this regard is the representation of the muscles in the cerebral
cortex, i.e., motor homunculus, where the most pertinent question is whether cortical
muscles' representations do exist at all or only synergies and movement characteristics
are encoded in the cortex (Schieber, 2001). There is also a considerable difference
in the amount of studies of distal and proximal muscles with very few studies addressing
the question of the somatotopical interaction of the proximal muscles cortical representations
(Kocak et al., 2009; Kesar et al., 2018).
Most readers are likely to be familiar with the picture from textbooks on how the
motor homunculus is presented in the brain (Kocak et al., 2009) and there is a lot
of data on the brain's plasticity (Nobre, 2001; Nazarova and Blagovechtchenski, 2015).
It is sufficient to mention the so-called “mirror system” effect, where the excitability
thresholds for TMS of the individual muscle vary depending on the observed movements,
in order to emphasize how motor maps can dynamically change their presentations in
the cortex (Buccino et al., 2004). Also of note is that the direct connection of the
cortical neurons with the spinal motor neurons does not necessarily mean direct activation
effect: the activity of the upper motor neuron does not always uniquely correlate
with the activity of the lower motor neuron to which it is projected (Lemon et al.,
1998; Lemon, 2008; Nazarova and Blagovechtchenski, 2015).
To our knowledge, it has not yet been investigated how cortical representation of
a particular muscle can be associated with the possibility of its functional reconstruction
in situation when the biomechanical position of this muscle is changed. Indeed, there
is always a chance for the pathological plasticity leading to irrelevant movements
and/or pain. It is generally known that some muscles have smaller cortical representation,
and accordingly, less cortical voluntary control. Also we showed recently that there
is a change in the basic EEG rhythms in children with arthrogryposis (Blagoveschenskiy
et al., 2018), which can also be a reflection of the plastic changes in the motor
cortex. Perhaps functional mapping of the cortical representations of the possible
donor's muscles may give a better answer to the question–which of the donor muscles
is most suitable for such an operation. How can one estimate the plasticity of a motor
representation? We believe that the combination of non-invasive neuroimaging and stimulation
approaches may allow exploring this issue more systematically. The degree of the involvement
of cortical motor representations during muscle contraction can be assessed using
MEG, EGG, and fMRI (Hopfinger et al., 2001). Fundamental in this case is the change
in neuronal activity as a result of short-term motor learning. At the same time, it
is necessary to estimate the corticospinal efficacy for such central rearrangements
using a non-invasive stimulation approach, such as TMS.
How to Facilitate Recovery and Rehabilitation Processes After Autotransplantation?
After muscle autotransplantation, many peripheral and central changes occur affecting
all receptors and neurons associated with the movement process which is modified by
surgery. One of the most interesting aspects of this problem is how to “explain” to
the brain how to deal with those new degrees of freedom and control—i.e., elbow flexion—for
which the brain had no control before.
A contemporary understanding of the movement organization includes such basic elements
as the solution of an inverse problem, the formation of an efferent copy of the movement,
which allow the brain comparing the planned motor pattern with the results of the
performed action (Gallivan et al., 2018). However, in patients with arthrogryposis,
there are no formed sensorimotor pattern associated with elbow flexion, or processing
of the corresponding afferent signals and their comparison with an efferent copy.
When a muscle is transplanted, the situation becomes even more complicated since the
muscles get new biomechanical positions.
In order to solve these problems, we propose to use not only postoperative rehabilitation
but also a preoperative training aimed at the formation of central commands leading
to the consolidation of new neurobiomechanical patterns functionally associated with
the activation of a donor muscle. For example, let us consider a case of the donor
muscle being latissimus dorsi, the activation of which is normally does not lead to
elbow flexion. We propose to ask a patient to perform the contraction of this muscle
even before the operation, which, of course, at this stage does not yet results in
the flexion of the arm (Figure 1). However, we can use the electromyogram from the
contracted muscle as a control signal to trigger a prosthesis that performs a mechanical
elbow flexion. Thus, we do not require the patient to exercise their own flexion,
we rather hypothesize that as a result of this training, there would be an association
between the formation of the central motor command for the mechanical elbow flexion
and the contraction of the future donor muscle–latissimus dorsi muscle in this case
(see Figure 1). After the surgery, when the latissimus dorsi muscle is in the position
of the bicep brachii, the patient is asked again to execute a contraction of latissimus
dorsi which for the first time would be associated with the elbow flexion. Initially
after the recovery, these attempts will have an assistance of the prosthesis which
later can be removed.
Figure 1
A general scheme for the use of prosthesis in the course of pre- and postoperative
training. (A) Pre-operative training. A prosthesis is controlled by the EMG originating
from the contraction of the donor muscle. (1) Donor muscle (2) Contraction of the
donor muscle (3) EMG at baseline period (4) Control Signal (5) Prosthesis (6) Flexion
produced by prosthesis. (B) Surgical intervention (7) Muscle transplantation. The
muscle and its nerves are transplanted from their original location to a new location
to perform a function of biceps brachii. (C) Post-operative training. A motor rehabilitation
continues with a donor muscle being in a new place with the assistance of the prosthesis.
(8) Donor muscle in the target position (9) New EMG baseline (10) Control Signal (11,
12) Flexion with the donor muscle plus assistance from the prosthesis (13) Flexion
produced by the donor muscle without the assistance from the prosthesis.
At the present moment it is not known what may be the effect of the described preoperative
training on the speed of the rehabilitation. Developing this new approach would require
creating a simple prosthesis that performs an elbow flexion depending on the activity
of the donor's muscles, which will be placed at the biceps brachii position. Importantly,
already before the surgical intervention, an association should be formed in the brain
between the contraction of the donor's muscle and the elbow flexion. Practical implementations
would include the creation of a simple exoskeleton robot which controls the flexion
of the arm in the special joint (in this case, the elbow), depending on the electromyogram
of the muscle selected for the transplantation. In addition, in the initial pre-operative
period, such robot-exoskeleton will control proper flexion, until the neuromotor patterns
are stabilized. According to our observation, patients after the surgery prefer to
contract the muscle isometrically, without changing the joint angle. We believe that
using the described approach, it would be possible to avoid the dominance of the central
descending commands which do not result in a flexor movement, since the electromyogram
of the donor muscle will be used to perform the flexion. In a future prosthesis, the
flexion would be launched only when a certain pattern on an EMG is reached that differs
from the pattern corresponding to a simple isometric movement.
In conclusion, we suggest that:
The study of the cortical representations in the central nervous system of the muscles
before their transplantation to a new position may play an important role in selecting
the donor muscles.
Pre-operative training of the new biomechanical synergies based on the EMG activity
from the donor muscle will allow speeding up the rehabilitation process.
Author Contributions
All authors listed have made a substantial, direct and intellectual contribution to
the work, and approved it for publication.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial
or financial relationships that could be construed as a potential conflict of interest.