Structure-function relationships in the rat brainstem subnucleus interpolaris: VI. Cervical convergence in cells deafferented at birth and a potential primary afferent substrate.

Abstract

Possible substrates for peripheral injury-induced receptive field (RF) changes were assessed in the trigeminal (V) subnucleus interpolaris (SpVi). In adult rats with infraorbital nerve section at birth, 449 cells were studied ipsilateral to the lesion by using electrophysiological methods. Of these, 33 (7.4%) had RFs that included facial vibrissae, guard hairs, and skin, as well as ipsilateral regions normally innervated by cervical primary afferents (ear, neck, shoulder, arm, forepaw). Such non-V convergence was never seen in 373 normal SpVi cells or in 641 V ganglion cells ipsilateral to the lesion. SpVi cells with cervical RFs discharged to V ganglion shocks and their latencies (1.6 +/- 0.7 ms, mean +/- s.d.) did not differ from normal (1.4 +/- 0.5). Most (71%) projected to the thalamus. None were nociceptive-biased, and many had unusually discontinuous RFs (48%). Possible pathways by which cervical inputs might reach SpVi neurons were investigated in additional anatomical and electrophysiological experiments. Eight SpVi cells with cervical RFs were intracellularly labeled with HRP. Although all had dendrites that were polarized toward SpVi regions containing spared mandibular and/or ophthalmic primary afferents, none had dendrites which extended out of SpVi. In other neonatally nerve-damaged adults, WGA-HRP was injected bilaterally into forepaw, arm, and shoulder regions. Transganglionic transport was restricted to normal targets. However, WGA-HRP injections into SpVi retrogradely labeled a total of 46 +/- 20 (mean +/- s.d.) cells in ipsilateral C1-3 dorsal root ganglia, and 24 +/- 8 cells in C4-8 ganglia. In controls, labeled cells were seen only in C1-3 ganglia (32 +/- 9). The distribution and number of labeled cells in the somatosensory cortex did not differ in experimental and control cases. No labeled cells were visible in the dorsal column nuclei of either the normal or experimental rats. Thus, retrograde labeling studies suggest that a cervical primary afferent projection to SpVi is a potential substrate for cervical convergence expressed in neonatally deafferented SpVi cells.