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. 2020 Oct 9:14:555593.
doi: 10.3389/fnsys.2020.555593. eCollection 2020.

Mapping of the Spinal Sensorimotor Network by Transvertebral and Transcutaneous Spinal Cord Stimulation

Polina Shkorbatova  1   2 , Vsevolod Lyakhovetskii  2   3 , Natalia Pavlova  1   2 , Alexander Popov  2 , Elena Bazhenova  1   2 , Daria Kalinina  1 , Oleg Gorskii  1   2   3 , Pavel Musienko  1   2   3   4
Affiliations

Mapping of the Spinal Sensorimotor Network by Transvertebral and Transcutaneous Spinal Cord Stimulation

Polina Shkorbatova et al. Front Syst Neurosci. .

Abstract

Transcutaneous stimulation is a neuromodulation method that is efficiently used for recovery after spinal cord injury and other disorders that are accompanied by motor and sensory deficits. Multiple aspects of transcutaneous stimulation optimization still require testing in animal experiments including the use of pharmacological agents, spinal lesions, cell recording, etc. This need initially motivated us to develop a new approach of transvertebral spinal cord stimulation (SCS) and to test its feasibility in acute and chronic experiments on rats. The aims of the current work were to study the selectivity of muscle activation over the lower thoracic and lumbosacral spinal cord when the stimulating electrode was located intravertebrally and to compare its effectiveness to that of the clinically used transcutaneous stimulation. In decerebrated rats, electromyographic activity was recorded in the muscles of the back (m. longissimus dorsi), tail (m. abductor caudae dorsalis), and hindlimb (mm. iliacus, adductor magnus, vastus lateralis, semitendinosus, tibialis anterior, gastrocnemius medialis, soleus, and flexor hallucis longus) during SCS with an electrode placed alternately in one of the spinous processes of the VT12-VS1 vertebrae. The recruitment curves for motor and sensory components of the evoked potentials (separated from each other by means of double-pulse stimulation) were plotted for each muscle; their slopes characterized the effectiveness of the muscle activation. The electrophysiological mapping demonstrated that transvertebral SCS has specific effects to the rostrocaudally distributed sensorimotor network of the lower thoracic and lumbosacral cord, mainly by stimulation of the roots that carry the sensory and motor spinal pathways. These effects were compared in the same animals when mapping was performed by transcutaneous stimulation, and similar distribution of muscle activity and underlying neuroanatomical mechanisms were found. The experiments on chronic rats validated the feasibility of the proposed stimulation approach of transvertebral SCS for further studies.

Keywords: decerebrated rat; neuromodulation; sensorimotor network; spinal cord; transcutaneous stimulation; transvertebral spinal cord stimulation.

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Figures

FIGURE 1
FIGURE 1
(A) Design of the experiment. The decerebrate rat is fixed in the custom stereotaxic frame and the holes were drilled in the spinous processes of the VT12–VS1 (red dots) vertebrae. The stimulating vertebral electrode was placed alternately in the hole in each vertebra. The stimulating cutaneous electrode was placed in the zones between adjacent vertebrae. The intramuscular electrodes were implanted to record EMG signals. (B) The representative scheme of the frontal section of vertebra VL2 with the spinal cord, dorsal (red) and ventral (green) roots, and dorsal root ganglia (DRGs, pink) inside the vertebral canal. The position of the stimulating cutaneous electrode and vertebral electrode in the spinous process is shown. The contact insulation-free area of the vertebral electrode indicated with a red arrow. (C) An example of motor-evoked potential with the main characteristics measured. (D) An example of motor-evoked potential to first (blue) and second (red) pulse of double-pulse stimulation. (E,F) The recruitment curves of motor (E) and sensory (F) responses at stimulation of different vertebrae and their slopes (max, maximal slope; i, slope at stimulation of some other vertebra).
FIGURE 2
FIGURE 2
The representative examples of evoked potential dynamics with increasing current for transvertebral double-pulse electrical stimulation (1,900–2,200 μA) delivered at VL5 vertebrae for mm. flexor hallucis longus (FHL) and soleus (SOL). Stim, stimulation impulse; ER, early response; MR, medium response.
FIGURE 3
FIGURE 3
The examples of averaged evoked potentials (SE plotted by dotted line) (A) and the latencies (B) and threshold currents (C) of early responses of mm. longissimus dorsi (LD), abductor caudae dorsalis (ACD), iliacus (IL), adductor magnus (ADD), vastus lateralis (VL), semitendinosus (ST), tibialis anterior (TA), gastrocnemius medialis (GM), soleus (SOL), and flexor hallucis longus (FHL) at maximal or submaximal current at “optimal” stimulation. **p < 0.01, *p < 0.05.
FIGURE 4
FIGURE 4
Examples of the recruitment curves for mm. longissimus dorsi (LD), abductor caudae dorsalis (ACD), iliacus (IL), adductor magnus (ADD), vastus lateralis (VL), semitendinosus (ST), tibialis anterior (TA), gastrocnemius medialis (GM), soleus (SOL), and flexor hallucis longus (FHL) plotted for motor and sensory responses in the same animal when the electrical stimulation was delivered at the VT12–VS1 vertebrae.
FIGURE 5
FIGURE 5
The mean skeletotopy of spinal cord segments in relation to the VT12–VS1 vertebrae (the T11–S1 segments, their roots, and DRGs are marked by different colors corresponding to Figure 2) versus the averaged distributions of normalized slopes for mm. longissimus dorsi (LD), abductor caudae dorsalis (ACD), iliacus (IL), adductor magnus (ADD), vastus lateralis (VL), semitendinosus (ST), tibialis anterior (TA), gastrocnemius medialis (GM), soleus (SOL), and flexor hallucis longus (FHL) at the stimulation of these vertebrae. Motor responses (blue), sensory responses (red). The length of all vertebrae presented are equalized for simplicity.
FIGURE 6
FIGURE 6
The motor-evoked potentials triggered by transvertebral stimulation in chronic animals. (A) Example of evoked potential recruitment dynamics with increasing current (1,600–2,000 μA) for m. Tibialis anterior (TA). (B) The individual recruitment curves for mm. TA and gastrocnemius medialis (GM) of different chronic rats. Stim, stimulation impulse; ER, early response; MR, medium response.
FIGURE 7
FIGURE 7
Examples of evoked potential dynamics with increasing current for transcutaneous double-pulse electrical stimulation (3,400–3,700 μA) delivered at the zone between VL2 and VL3 vertebra for mm. vastus longus (VL) and soleus (SOL). Stim, stimulation impulse; ER, early response; MR, medium response; LR, late response.
FIGURE 8
FIGURE 8
The relative slopes of recruitment curves in (A) transvertebral stimulation of VT12, VL2, and VL6 and (B) transcutaneous stimulation of VT12–VT13, VL2–VL3, and VL6–VS1 zones of mm. longissimus dorsi (LD), abductor caudae dorsalis (ACD), iliacus (IL), adductor magnus (ADD), vastus lateralis (VL), semitendinosus (ST), tibialis anterior (TA), gastrocnemius medialis (GM), soleus (SOL), and flexor hallucis longus (FHL).
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