Segmental neuropathic pain does not develop in male rats with complete spinal transections

Abstract

In a previous study using male rats, a correlation was found between the development of "at-level" allodynia in T6-7 dermatomes following severe T8 spinal contusion injury and the sparing of some myelinated axons within the core of the lesion epicenter. To further test our hypothesis that this sparing is important for the expression of allodynia and the supraspinal plasticity that ensues, an injury that severs all axons (i.e., a complete spinal cord transection) was made in 15 male rats. Behavioral assessments were done at level throughout the 30-day recovery period followed by terminal electrophysiological recordings (urethane anesthesia) from single medullary reticular formation (MRF) neurons receiving convergent nociceptive inputs from receptive fields above, at, and below the lesion level. None of the rats developed signs of at-level allodynia (versus 18 of 26 male rats following severe contusion). However, the terminal recording (206 MRF neurons) data resembled those obtained previously post-contusion. That is, there was evidence of neuronal hyper-excitability (relative to previous data from intact controls) to high- and low-threshold mechanical stimulation for "at-level" (dorsal trunk) and "above-level" (eyelids and face) cutaneous territories. These results, when combined with prior data on intact controls and severe/moderate contusions, indicate that (1) an anatomically incomplete injury (some lesion epicenter axonal sparing) following severe contusion is likely important for the development of allodynia and (2) the neuronal hyper-excitability at the level of the medulla is likely involved in nociceptive processes that are not directly related to the conscious expression of pain-like avoidance behaviors that are being used as evidence of allodynia.

FIG. 1.

Typical examples of stimulus-response characteristics in medullary reticular formation (MRF) neurons from spinally transected animals. (A) Example of excitatory responses of a single MRF neuron located in the left nucleus reticularis gigantocellularis pars alpha to low-threshold stimulation of dorsal trunk, face and eyelid. As shown, this neuron responded to gentle pinching of the ear (search stimulus). (B) Example of excitatory responses of another single MRF neuron located in the left nucleus reticularis gigantocellularis to high-threshold stimulation of dorsal trunk, face, and eyelid. This neuron did not respond to low-threshold stimulation of trunk but responded to low-threshold stimulation of the face and eyelid. Horizontal bars indicate the onset and duration of the mechanical stimulus.