Morphology of primary somatosensory cortical neurons receiving input from the tooth pulp

1. To elucidate the morphological and electrophysiological characteristics of tooth pulp-driven neurons (TPNs) in the primary somatosensory cortex (SI), we injected neurobiotin into TPNs whose electrophysiological characteristics had been identified. 2. TPNs, responsive to electrical stimulation of the tooth pulp, were recorded intracellularly and injected from areas 3a and 3b of SI. A total of 58 TPNs in SI were successfully injected and reconstructed. Nineteen of these TPNs were located in area 3a and 39 in area 3b. Three area 3a TPNs were identified in lamina II, eight in lamina III, seven in lamina V, and one in lamina VI. Five 3b TPNs were identified in lamina II, 19 in lamina III, 7 in lamina IV, 7 in lamina V, and 1 in lamina VI. 3. Thalamic and tooth pulp latencies of lamina III and IV TPNs were shorter than those of lamina II and V TPNs. On the other hand, lingual and masseteric nerve latencies of TPNs were not consistent with thalamic and tooth pulp latencies. 4. Three of 19 area 3a TPNs and 7 of 39 area 3b TPNs were classified as pulp-specific TPNs, which received only tooth pulp input. Thirteen of 19 area 3a TPNs and 24 of 32 area 3b TPNs were classified as low-threshold mechanoreceptive TPNs, which responded to nonnoxious mechanical stimulation of the receptive field, and only 2 area 3b TPNs were classified as wide-dynamic range TPNs. Six of the area 3a TPNs and 14 of the area 3b TPNs responded to electrical stimulation of the lingual and/or masseteric nerves. Nociceptive-specific TPNs were not recorded in this study. 5. Lamina II TPNs in areas 3a and 3b had small somata, and those in area 3a had dendrites spreading into laminae I-II. Two TPNs in area 3a had axon collaterals extending into area 4. In contrast, area 3b TPNs in lamina II have dendrites spreading into laminae I-III. Their axons did not extend deeply into the subcortical regions, and the axon collaterals reached into area 3a. 6. Lamina III TPNs were classified according to their morphological characteristics as pyramidal or nonpyramidal stellate TPNs. Pyramidal lamina III TPNs had typical pyramidal somata, like those of lamina V pyramidal cells. Furthermore, those in areas 3a and 3b had dendrites with numerous spines spreading into laminae I-III, and some of the area 3a TPNs have axons with collaterals projecting into area 4. Lamina III area 3b TPNs had morphological properties similar to those in area 3a. 7. Lamina IV TPNs were recorded only from area 3b. Their somata were similar in size to those of lamina III TPNs and had dendrites with many tufts. All lamina IV TPNs had axon collaterals running around the soma, but the axons were not clearly seen to extend into the subcortical white matter. 8. Lamina V TPNs in area 3a had typical pyramidal somata and their basal dendrites spread into laminae IV- VI. They had large somata with apical dendrites spreading widely into laminae I-IV and axons with collaterals reaching into the white matter. Laminae V TPNs in area 3a had morphological features similar to those in area 3b. 9. The present data suggest that area 3a and 3b TPNs in each lamina have similar morphological properties, but that TPNs in different laminae also differ morphologically, relaying tooth pulp sensory information to neurons in the same or other cortical areas with different output systems.