Spinothalamic tract neurons that project to medial and/or lateral thalamic nuclei: Evidence for a physiologically novel population of spinal cord neurons

On the basis of the thalamic area to which they project as determined with the antidromic activation technique, lumbosacral spinothalamic neurons in anesthetized monkeys were classified as medial (M-STT), lateral (L-STT), or lateral-medial (LM-STT) spinothalamic tract cells. M-STT cells projected only to the medial thalamus (central lateral nucleus or adjacent parts of the medial dorsal nucleus), L-STT cells projected only to the lateral thalamus (ventral posterior lateral nucleus), and LM-STT cells projected to both lateral and medial thalamic nuclei. LM- and L-STT cells were indistinguishable in their response characteristics. Sixty-eight percent were wide dynamic range cells (activated by innocuous mechanical stimuli, but more powerfully by noxious stimuli). Twenty-seven percent were high-threshold cells (responding only to noxious or near-noxious stimuli). Five percent were classified as deep (activated by proprioceptive stimuli). In the majority of cases LM- and L-STT cells had excitatory receptive fields that were restricted to the ipsilateral hindlimb and were powerfully activated by volleys in cutaneous A- and C-fibers. Both cell classes had widely distributed inhibitory receptive fields; were found in similar locations in the dorsal horn, and had axons with comparable conduction velocities. The response properties of M-STT cells differed substantially from those of both LM- and L-STT cells. Sixty-two percent were classified as high-threshold, 25% as wide dynamic range, and 12% as deep neurons. The excitatory receptive fields of most M-STT cells included parts of several limbs or even the entire surface of the body and face. Responses to volleys in cutaneous A- and C-fibers were weak, and M-STT cells rarely had inhibitory receptive fields. M-STT cells were commonly found in the intermediate zone or ventral horn. The axons of M-STT cells had slower conduction velocities than did those of LM- or L-STT cells. For LM-STT cells, it could be calculated that almost 90% of the time spent by an action potential ascending from the cell body is spent in the portion of the axon caudal to the point at which the medially and laterally directed branches arose from the parent axon. Evidence was found that there are additional collaterals issuing from such axons at the level of the bulbar reticular formation. Antidromic activation was interrupted for three LM-STT and three M-STT cells by restricted lesions of the spinal cord white matter at an upper cervical level. The positions of the axons were inferred to be in the lateral funiculus for all the neurons except one M-STT cell, whose axon was in the ventral funiculus. Lesions of the lateral funiculi at an upper cervical level reduced the sizes of the excitatory receptive fields of M-STT cells from all of the body and face to just the ipsilateral hindlimb in five of six neurons tested. Electrical stimulation within the medial reticular formation of the pons and medulla produced an excitation of M-STT cells that outlasted the stimulus, a discharge comparable to that produced by noxious stimulation of the skin. Lesions of the spinal cord that disrupted the descending excitation also reduced the size of the excitatory receptive field. These findings suggest that the large excitatory receptive fields of M-STT cells may depend on a neural pathway involving ascending tracts that activate neurons of the reticular formation. These neurons then excite M-STT cells by way of reticulospinal volleys.