Spinothalamic and spinohypothalamic tract neurons in the sacral spinal cord of rats .1. Locations of antidromically identified axons in the cervical cord and diencephalon

1. A goal of this study was to determine the sites in the diencephalon to which neurons in sacral spinal segments of rats project. Therefore, 95 neurons were recorded extracellularly in spinal segments L(6)-S-2 Of rats that were anesthetized with urethan. These neurons were activated initially antidromically with currents less than or equal to 30 mu A from a monopolar stimulating electrode placed into the contralateral posterior diencephalon. The mean +/- SE current for antidromic activation from these sites was 16 +/- 0.8 mu A. These neurons were recorded in the superficial dorsal horn (4%), deep dorsal horn (89%), and intermediate zone and ventral horn (4%). 2. Systematic antidromic mapping techniques were used to map the axonal projections of 41 of these neurons within the diencephalon. Thirty-three neurons (80%) could be activated antidromically with currents less than or equal to 30 mu A only from points in the contralateral thalamus and are referred to as spinothalamic tract (STT) neurons. Eight neurons (20%) were activated antidromically with low currents from points in both the contralateral thalamus and hypothalamus, and these neurons are referred to as spinothalamic tract/spinohypothalamic tract (STT/SHT) neurons. Three additional neurons were activated antidromically with currents less than or equal to 30 mu A only from points within the contralateral hypothalamus and are referred to as spinohypothalamic tract (SHT) neurons. The diencephalic projections of another 51 neurons were mapped incompletely. These neurons are referred to as spinothalamic/unknown (STT/U) neurons to indicate that it was not known whether their axons ascended beyond the site in the thalamus from which they initially were activated antidromically. 3. For 31 STT neurons, the most anterior point at which antidromic activation was achieved with currents less than or equal to 30 mu A was determined. Fourteen (45%) were activated antidromically only from sites posterior to the ventrobasal complex (VbC) of the thalamus. Sixteen STT neurons (52%) were activated antidromically with low currents from sites at the level of the VbC, but not from more anterior levels. One STT neuron (3%) was activated antidromically from the anteroventral nucleus of the thalamus. 4. STT/SHT neurons were antidromically activated with currents less than or equal to 30 mu A from the medial lemniscus (ML), anterior pretectal nucleus (Apt), posterior nuclear group and medial geniculate nucleus (Po/MG), and zona incerta in the thalamus and from the optic tract (OT), supraoptic decussation, or lateral area of the hypothalamus. No differences in the sites in the thalamus from which STT and STT/SHT neurons were activated antidromically were apparent. Five STT/SHT neurons (62%) were activated antidromically from points in the thalamus in the posterior diencephalon and from points in the hypothalamus at more anterior levels. Three STT/SHT neurons (38%) were activated antidromically with currents less than or equal to 30 mu A from sites in both the thalamus and hypothalamus at the same anterior-posterior level of the diencephalon. All three of these STT/SHT neurons projected to the intralaminar nuclei (parafascicular or central lateral nuclei) of the thalamus. 5. Seven STT/SHT neurons were tested for additional projections to the ipsilateral brain. Two (29%) were activated antidromically with currents less than or equal to 30 mu A and at longer latencies from sites in the ipsilateral diencephalon. One could only be activated antidromically from the hypothalamus ipsilaterally. The other was activated antidromically at progressively increasing latencies from points in the ipsilateral brain that extended as far posteriorly as the posterior pole of the MG. 6. Fifty-eight STT, STT/SHT, and STT/U neurons were classified as low-threshold (LT), wide dynamic range (WDR), or high-threshold (HT) neurons based on their responsiveness to innocuous and noxious mechanical stimuli applied to their cutaneous receptive fields. There were no statistically significant differences among the numbers of LT, WDR, and HT neurons categorized as STT or STT/SHT neurons. For STT neurons, the most anterior points from which LT neurons were activated antidromically with low currents were located in and adjacent to the VbC. In contrast, the most anterior points from which nociceptive (WDR and HT) neurons were activated antidromically tended to be located posterior to the VbC in the ML, Apt, OT, and Po/MG. This difference in the apparent termination patterns of LT and nociceptive (WDR and HT) STT neurons was statistically significant. 7. STT and STT/SHT neurons also were tested for their responsiveness to either colorectal (CrD) or vaginal (VaD) distention, or to both. Nine of 23 STT neurons (39%) and three of four STT/SHT neurons (75%) were excited by CrD. Five of 14 STT neurons (36%) and two of four STT/SHT neurons (50%) were excited by VaD. Four STT and two STT/SHT neurons were excited by both CrD and VaD and two STT neurons were excited by CrD but not VaD. There were no statistically significant differences among the numbers of STT and STT/SHT neurons that were excited by either CrD or VaD. 8. Using a second stimulating electrode, 80 STT, STT/SHT, and STT/U neurons also were activated antidromically with currents less than or equal to 30 mu A from the contralateral white matter of upper cervical segments. More than 90% of these neurons were activated from the lateral half of the contralateral lateral funiculus. Twenty-two of these neurons were activated antidromically from both C-4 and C-2. At all cervical levels, the majority was activated antidromically from the ventrolateral funiculus (VLF). No segregation of axons in the dorsolateral funiculus or VLF according to diencephalic projections, recording site, or physiological classification was apparent. 9. Conduction velocities from the recording point to sites in C-4, C-2, and the brain from which STT, STT/SHT, and STT/U neurons were activated antidromically were calculated. The mean +/- SE conduction velocity to C-4 was 22.5 +/- 1.0 m/s, to C-2 was 21.5 +/- 1.9 m/s, and to the initial low-threshold point in the brain was 19.8 +/- 0.9 m/s. The mean conduction velocity to the brain was significantly slower than those to C-4 and C-2. The mean conduction velocities to C-4 and C-2 were nut significantly different. IO. Our findings demonstrate that neurons in spinal segments L(6)-S-2 Of rats issue axons that ascend contralaterally through the lateral white matter in cervical segments and project to widespread areas of the thalamus and hypothalamus, Many respond to nociceptive cutaneous stimuli and visceral stimuli. Thus sacral STT and STT/SHT neurons are capable of transmitting information about somatic and visceral stimuli arising in the perineum and pelvis directly to areas of the thalamus and hypothalamus involved in the processing of such information. Our finding's also demonstrate differences in the patterns of the diencephalic projections of sacral neurons according to their physiological responsiveness. For exam; pie, sacral STT neurons that respond preferentially to innocuous mechanical stimuli appear to project almost exclusively to the VbC. In contrast, nociceptive sacral STT neurons project to several thalamic nuclei, and the majority seem to terminate in areas that are posterior to the VbC.