Structure-function relationships in rat brain stem subnucleus interpolaris. IX. Inputs from subnucleus caudalis

1. In an accompanying paper, Jacquin et al. (1990) described the effects of cortical ablation on the receptive-field (RF) properties of neurons in spinal trigeminal (SpV) subnucleus interpolaris (SpVi). A similar ablation paradigm was used here to clarify the role of an additional source of SpVi RF modulation, the extensive projection from caudally adjacent subnucleus caudalis (SpVc). 2. Intra- and extracellular recording, electrical stimulation, and RF mapping techniques were used to study the responses and projections of 356 SpVi cells in 11 rats 58-141 days after surgical isolation of SpVc from SpVi. This was achieved by a transverse knife cut through the lateral one-half of the left medulla just caudal to the obex. Because this lesion serves trigeminal (V) primary afferents caudal to SpVi, as well as postsynaptic intersubnuclear axons traversing to and from SpVi, kainic acid was used in other animals to selectively lesion SpVc inputs to SpVi. Seven rats received kainic acid injections into SpVc 5-28 days before providing similar electrophysiological data on 300 SpVi cells. Results were compared with that of 330 cells from 9 normal adult rats. 3. Knife-cut or kainic-acid lesions did not alter the topography of SpVi cells or the RF properties of 71 ipsilateral V primary afferents. However, both types of lesions produced the same profound changes in the response character of SpVi cells. Statistically reliable increases were found in the relative percentages of cells that 1) expressed convergence from multiple receptor organs, 2) were unresponsive to mechanical stimulation of orofacial regions, 3) responded tonically to a maintained peripheral stimulus, 4) were spontaneously active, 5) were directionally sensitive, 6) responded to stimulation of body surfaces innervated by cervical primary afferents, and 7) had split RFs. 4. RFs were also reliably larger for whisker-activated local circuit and projection neurons after both types of lesions. Over one-third of this local circuit group responded to more than one whisker in both experimental groups, whereas in normals all responded to one whisker. 5. All other SpVi response indices were unchanged by SpVc lesions. The most notable negative result was a normally low percentage of cells that were responsive to nociceptive stimuli. 6. To assess whether these RF changes reflected altered collateral morphology of V primary afferents in SpVi, whisker (n = 11) and guard-hair- (n = 7) activated axons were stained with horseradish peroxidase rostral to knife-cut or kainic-acid lesions. Morphometric analyses revealed no differences from normal suggesting that V primary afferents to not sprout or expand their arbors in SpVi after partial target removal (SpVc kainic acid) or axotomy of their more distal process (SpVc knife cut). 7. Our data suggest that under barbiturate anesthesia SpVc inputs contribute to RF size and character, base-line activity, and the probability of having a RF in a substantial number of SpVi cells. Some effects of SpVc lesions were similar to that of cortical ablation. Others, such as effects on adaptation properties, directional sensitivity, base-line activity, RF continuity, and projection neuron RF size were unique to SpVc lesions. Thus SpVc serves both facilitatory and inhibitory functions in SpVi RF synthesis. However, SpVc does not appear to contribute to nociceptive responsiveness in SpVi.