A Review on Locomotor Training after Spinal Cord Injury: Reorganization of Spinal Neuronal Circuits and Recovery of Motor Function

Andrew C Smith, Maria Knikou, Andrew C Smith, Maria Knikou

Abstract

Locomotor training is a classic rehabilitation approach utilized with the aim of improving sensorimotor function and walking ability in people with spinal cord injury (SCI). Recent studies have provided strong evidence that locomotor training of persons with clinically complete, motor complete, or motor incomplete SCI induces functional reorganization of spinal neuronal networks at multisegmental levels at rest and during assisted stepping. This neuronal reorganization coincides with improvements in motor function and decreased muscle cocontractions. In this review, we will discuss the manner in which spinal neuronal circuits are impaired and the evidence surrounding plasticity of neuronal activity after locomotor training in people with SCI. We conclude that we need to better understand the physiological changes underlying locomotor training, use physiological signals to probe recovery over the course of training, and utilize established and contemporary interventions simultaneously in larger scale research studies. Furthermore, the focus of our research questions needs to change from feasibility and efficacy to the following: what are the physiological mechanisms that make it work and for whom? The aforementioned will enable the scientific and clinical community to develop more effective rehabilitation protocols maximizing sensorimotor function recovery in people with SCI.

Figures

Figure 1
Figure 1
Modulation of neuronal activity while walking in uninjured humans. (a, b) Soleus H-reflexes and soleus motor evoked potentials (MEPs) amplitude at each bin of the step cycle while stepping on a motorized treadmill for single subjects (a) and for a group of healthy subjects (b). (c, d) Short-latency tibialis anterior (TA) flexor reflexes and TA MEPs amplitude at each bin of the step cycle while stepping on a motorized treadmill for single subjects (c) and for a group of healthy subjects (d). For the grouped data, for each bin of the step cycle, the soleus H-reflex was normalized to the maximal M-wave evoked 60–80 ms after the test H-reflex, and the short-latency TA flexor reflexes and soleus/TA MEPs were normalized to the maximum homonymous locomotor EMG having subtracted the control EMG (EMG without stimulation) at identical time windows and bins. Each step was divided into 16 equal bins based on the signal from the right foot switch. Bin 1 corresponds to heel contact. Bins 8, 9, and 16 correspond approximately to stance-to-swing transition, swing initiation, and swing-to-stance transition, respectively. Vertical dotted lines designate the stance-to-swing transition phase. Data adopted and modified from [2, 16, 21, 22].
Figure 2
Figure 2
Functional reorganization of homosynaptic depression after locomotor training in SCI. (a) Schematic diagram of the soleus H-reflex homosynaptic depression exerted at Ia-motoneuron synapse with repetitive activation of Ia afferents. (b). Nonrectified waveform averages of soleus H-reflexes recorded at different stimulation frequencies from one AIS B patient before and after locomotor training for both legs. The soleus H-reflex amplitude exhibited a strong stimulation frequency-dependent depression after locomotor training. Data adopted and modified from [72].
Figure 3
Figure 3
Functional reorganization of presynaptic inhibition of soleus Ia afferents after locomotor training in SCI. (a) Schematic diagram of the neuronal pathway of presynaptic inhibition of soleus Ia afferents. In this paradigm, presynaptic inhibition of soleus Ia afferents is induced by a conditioning afferent volley following common peroneal nerve stimulation at long conditioning-test (C-T) intervals. (b) Mean amplitude of the conditioned soleus H-reflex as a percentage of the unconditioned H-reflex recorded at each C-T interval tested before and after locomotor training from the right leg, grouped per AIS, in the seated position. ∗p < 0.05 indicate statistically significant differences of the conditioned H-reflexes recorded before and after locomotor training. Data adopted and modified from [72].
Figure 4
Figure 4
Functional reorganization of reciprocal Ia inhibition after locomotor training in SCI. (a) Schematic diagram of the neuronal pathway of reciprocal Ia inhibition mediated by a conditioning afferent volley induced by stimulation of the ipsilateral common peroneal nerve at short conditioning-test (C-T) intervals. (b) Mean amplitude of the conditioned soleus H-reflex as a percentage of the unconditioned H-reflex recorded at each C-T interval tested before and after locomotor training from the right leg, grouped per AIS, in the seated position. ∗p < 0.05 indicate statistically significant differences of the conditioned H-reflexes recorded before and after locomotor training. Data adopted and modified from [90].
Figure 5
Figure 5
Functional reorganization of nonreciprocal Ib inhibition after locomotor training in SCI. (a) Schematic diagram of the neuronal pathway of nonreciprocal Ib inhibition mediated by a conditioning afferent volley induced by stimulation of the ipsilateral medialis gastrocnemius nerve at short conditioning-test (C-T) intervals. The facilitatory locomotor Ib pathway is not indicated. (b) Mean amplitude of the conditioned soleus H-reflex as a percentage of the unconditioned H-reflex recorded at each C-T interval tested before and after locomotor training from the right leg, grouped per AIS, in the seated position. ∗p < 0.05 indicate statistically significant differences of the conditioned H-reflexes recorded before and after locomotor training. Data adopted and modified from [90].
Figure 6
Figure 6
Motor activity after locomotor training in incomplete and complete SCI. Nonrectified electromyographic (EMG) activity from 10 consecutive steps of medialis gastrocnemius (MG), tibialis anterior (TA), and peroneus longus (PL) muscles from the left legs in one motor incomplete SCI subject (AIS D) and in one motor complete SCI subject (AIS B) during assisted stepping after locomotor training. Note in subject R014 that MG and PL occur in a reciprocal pattern with the TA, but distinctive EMG bursts are absent in subject R06.

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