Inhibition and Facilitation of the Spinal Locomotor Central Pattern Generator and Reflex Circuits by Somatosensory Feedback From the Lumbar and Perineal Regions After Spinal Cord Injury

Abstract

Somatosensory feedback from peripheral receptors dynamically interacts with networks located in the spinal cord and brain to control mammalian locomotion. Although somatosensory feedback from the limbs plays a major role in regulating locomotor output, those from other regions, such as lumbar and perineal areas also shape locomotor activity. In mammals with a complete spinal cord injury, inputs from the lumbar region powerfully inhibit hindlimb locomotion, while those from the perineal region facilitate it. Our recent work in cats with a complete spinal cord injury shows that they also have opposite effects on cutaneous reflexes from the foot. Lumbar inputs increase the gain of reflexes while those from the perineal region decrease it. The purpose of this review is to discuss how somatosensory feedback from the lumbar and perineal regions modulate the spinal locomotor central pattern generator and reflex circuits after spinal cord injury and the possible mechanisms involved. We also discuss how spinal cord injury can lead to a loss of functional specificity through the abnormal activation of functions by somatosensory feedback, such as the concurrent activation of locomotion and micturition. Lastly, we discuss the potential functions of somatosensory feedback from the lumbar and perineal regions and their potential for promoting motor recovery after spinal cord injury.

Keywords: cutaneous; locomotion; lumbar; micturition; perineal; somatosensory feedback; spinal cord injury; spinal reflexes.

FIGURE 1

Modulation of hindlimb muscle activity and electrically evoked cutaneous reflexes when pinching the lumbar or perineal skin. (A) Each panel shows the electromyography (EMG) activity from the ipsilateral (I) and contralateral (C) semitendinosus (St, blue), lateralis gastrocnemius (LG, red), iliopsoas (IP, blue) and vastus lateralis (VL, red) while stimulating the superficial peroneal nerve before, during (in gray) and after pinch of the lumbar and perineal regions. The timing of the stimulation (Stim) is shown below the EMGs. Panels are from two representative cats. (B) Short-latency ipsilateral and contralateral reflex responses evoked by stimulating the superficial peroneal (SP) are shown for each period of the trial in selected hindlimb muscles. Waveforms are averages of 13–15 stimulations per period for a representative cat in an 80 ms window. To better visualize short-latency inhibitory responses, we superimposed averaged traces that received a stimulation (line in blue or red) with averaged traces without stimulation (line in gray). On the right, the results of reflex responses modulation of selected muscles with lumbar or perineal pinch are illustrated (↑, significant increase; ↓, significant decrease; ↔, non-significant difference in reflex responses). The figure is modified and reproduced with permission from Merlet et al. (2020, .

FIGURE 2

Schematic illustration of potential mechanisms modulating hindlimb locomotion and cutaneous reflexes with lumbar or perineal stimulation. Some potential mechanisms involved in the modulation of hindlimb locomotion and cutaneous reflexes, evoked by superficial peroneal (SP) nerve stimulation, with lumbar (blue) or perineal stimulation (red) are illustrated. Afferents from the SP nerve project to (1) spinal neurons and elicit reflex responses and to (2) a two-level central pattern generator (CPG) that includes rhythm generation (RG), and pattern formation (PF) levels. (3) Inputs from the perineal region primarily affect the PF level with weaker effects on the RG whereas (4) inputs from the lumbar region directly access the RG level. (5) The state of the spinal locomotor CPG controls the modulatory mechanism. (6) The modulatory mechanism controls neurotransmitter release of primary afferents from the SP nerve and the excitability of neurons within the reflex pathway. Inputs from the (7) perineal or (8) lumbar region projects to neurons that regulate the excitability of the modulatory mechanism. E, extensors; F, flexors; IN, interneurons; MN, motoneuron.