Sensitivity to painful and nonpainful electrocutaneous stimuli in monkeys: Effects of anterolateral chordotomy

Abstract

Four Macaca nemestrina monkeys were trained to pull a manipulandum to escape electrocutaneous stimulation (ES) applied to either leg. The intensities of stimulation which the monkeys chose to escape were those that humans identify as painful. The duration of escape trials was inversely related to stimulus intensity, and the force of escape responses was directly related to ES intensity. Reflexive responses were elicited by stimulus intensities below and above the escape threshold, and the force of the flexion reflexes was a negatively accelerating function of stimulus magnitude. The monkeys were also trained to respond, for water reinforcement, to cued, low-intensity ES. The stimulus intensities detected for water reinforcement were 50-100 x less than the escape thresholds. Following unilateral, anterolateral chordotomy, all monkeys demonstrated a large reduction in percentage of escape responding to stimulation of the contralateral leg. When the animals did escape contralateral stimulation, the latencies to respond were longer than preoperatively. The percentage and latency of escape responses to stimulation of the ipsilateral leg were not changed following chordotomy. Despite the depression of contralateral pain reactivity, the animals continued to respond to low levels of stimulation on the detection task, demonstrating that anterolateral chordotomy reduced the painfulness of strong stimulation without eliminating sensibility for low levels of stimulation. However, postoperative detection thresholds were consistently higher contralaterally than ipsilaterally. This effect resulted from slight contralateral decreases and significant ipsilateral increases in sensitivity to low levels of ES (relative to preoperative values). Thus, contralateral axons in the anterolateral column contribute to detection of light cutaneous stimulation, and chordotomy appears to disinhibit inputs from large myelinated afferent fibers to ipsilateral neurons in the spinal gray matter caudal to the lesion. The strictly contralateral slowing and reduction in percentage of pain reactivity by chordotomy correlated with reports from human patients. However, reflexive measures did not suffice as indicants of pain sensitivity. The chordotomies produced bilateral attenuations of reflexive amplitudes. Also, the force of operant escape responses was reduced with stimulation of either side. Thus, the disfacilitation of motoric reactions extended both rostral and caudal to the spinal lesions that interrupted propriospinal axons in the vicinity of the ventral horns.