An intracellular study of the synaptic input to sympathetic preganglionic neurones of the third thoracic segment of the cat

Abstract

In chloralose anaesthetized, paralyzed and artificially ventilated cats intracellular recordings were obtained from sympathetic preganglionic neurones (SPN) of the third thoracic segment of the spinal cord identified by antidromic stimulation of the white ramus T3. The synaptic input to SPNs was assessed, in cats with intact neuraxis or spinalized at C3, by electrical stimulation of segmental afferent fibres in intercostal nerves and white rami of adjacent thoracic segments and by stimulation of the ipsi- and contralateral dorsolateral funiculus and of the dorsal root entry zone of the cervical spinal cord. 1. (1) In both preparations SPNs showed on-going synaptic activity which predominantly consisted of excitatory post-synaptic potentials (EPSPs). Inhibitory post-synaptic potentials (IPSPs) were rarely observed. EPSPs were single step (5 mV) or, less frequently, large (up to 20 mV) summation EPSPs. The proportion of SPNs showing very low levels of on-going activity was markedly higher in spinal than in intact cats. 2. (2) Stimulation of somatic and sympathetic afferent fibres evoked early EPSPs (amplitude 3 mV, latency 5–22.3 ms), and late, summation EPSPs (amplitude up to 20 mV, latency 27–55 ms). Early and late EPSPs were evoked in nearly all SPNs in which this synaptic input was tested in the intact preparation (from 79–93% of the SPNs). In spinal cats, early EPSPs were evoked in 88% of the SPNs, whereas late EPSPs were recorded only in half of the neurones. No evidence for a monosynaptic pathway from these segmental afferent fibres to SPNs was obtained. 3. (3) In both intact and spinal cats, stimulation of the dorsolateral funiculus evoked early and late EPSPs in SPNs. Late EPSPs were recorded in 70% and 37% of the SPNs in intact and spinal cats, respectively. Early EPSPs, however, were evoked in all neurones. The early EPSPs evoked by stimulation of the dorsolateral funiculus had several components which are suggested to arise from stimulation of descending excitatory pathways with different conduction velocities. The following conduction velocities were calculated in intact (spinal) cats: 9.5–25 m/s (7.8–13.2 m/s), 5.7–9.5 m/s (5.5–7.8 m/s), 3.8–5.7 m/s (3.2–5.5 m/s), and 2.6–3.8 m/s (2.1–3.2 m/s). EPSPs of these various groups were elicited in a varying percentage in SPNs. EPSPs of the most rapidly conducting pathway were subthreshold for the generation of action potentials; some EPSPs of this group had a constant latency suggesting a monosynaptic pathway to SPNs. 4. (4) Stimulation of the dorsal root entry zone at the cervical level yielded essentially the same results as stimulation of the dorsolateral funiculus. EPSPs of the most rapidly conducting pathway, however, were rarely elicited by this stimulation, whereas late summation EPSPs were always evoked. 5. (5) Besides early and late EPSPs, stimulation of all synaptic inputs additionally evoked very late summation and single step EPSPs in intact and spinal cats, although in a smaller number of neurones. The very late summation EPSPs could be subdivided into two groups with latencies of 55–125 ms and 120–240 ms. The latter group was only observed in cats with an intact neuraxis. Very late single step EPSPs with latencies of 26–110 ms were evoked almost exclusively by spinal cord stimulation and are suggested to represent stimulation of a slowly conducting (0.5–1.2 m/s) descending excitatory pathway. 6. (6) IPSPs were only observed in a very small number of neurones by stimulation of these synaptic inputs. In any of these few SPNs, however, IPSPs were often evoked by more than one segmental input, but not by stimulation of spinal pathways. In two SPNs IPSPs were evoked in response to stimulation of the dorsal root entry zone; the conduction velocity of this descending inhibitory pathway was 2.2–2.6 m/s. 7. (7) A long-lasting membrane hyperpolarization (1–5 mV, 200–500 ms), associated with a reduction of the on-going synaptic activity and always preceded by a subthreshold EPSP, was recorded in SPNs in response to stimulation of all synaptic inputs. This hyperpolarization was preferentially observed in cats with an intact neuraxis. It was not affected by raising the intracellular chloride ion concentration. From these findings it is concluded that the synaptic input to SPNs is much greater than previously suspected from extracellular recordings. The rather homogeneous pattern of EPSPs evoked by all synaptic inputs does not allow a functional classification of SPNs of the third thoracic segment. Additionally, the existence of a fast and slowly conducting descending excitatory pathway onto SPNs was revealed.