J Neurophysiol (January 1, 2003). 10.1152/jn.00180.2002
Submitted on Submitted 11 March 2002; accepted in final form 13 September 2002

Excitatory Synaptic Currents in Lumbosacral Parasympathetic Preganglionic Neurons Evoked by Stimulation of the Dorsal Commissure

 ¹Department of Physiology, School of Medicine, Akita University, Akita 010-8543, Japan; and  ²Department of Pharmacology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania 15261

Miura, Akira, Masahito Kawatani, and William C. De Groat. Excitatory Synaptic Currents in Lumbosacral Parasympathetic Preganglionic Neurons Evoked by Stimulation of the Dorsal Commissure. J. Neurophysiol. 89: 382-389, 2003. Excitatory pathways from the dorsal commissure (DCM) to L₆-S₁ parasympathetic preganglionic neurons (PGN) were examined using whole-cell patch-clamp recording techniques in spinal cord slices from neonatal rats. PGN were identified by retrograde axonal transport of a fluorescent dye injected into the intraperitoneal space. Excitatory postsynaptic currents (EPSCs) were evoked in PGN by stimulation of DCM in the presence of bicuculline methiodide (10 µM) and strychnine (1 µM) to block inhibitory pathways. Electrical stimulation of DCM evoked two types of inward currents. In the majority of PGN (n = 66), currents (mean amplitude, 47.9 ± 4.7 pA) occurred at a short and relatively constant latency (3.8 ± 0.1 ms) and presumably represent monosynaptic EPSCs (Type 1). However, in other neurons (n = 20), a different type of EPSC (Type 2) was noted, consisting of a fast monosynaptic component followed by a prolonged inward current with superimposed fast transients presumably representing excitatory inputs mediated by polysynaptic pathways. Type 1 EPSCs were pharmacologically dissected into two components. A fast component was blocked by 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX, 5µM) and a slowly decaying component was blocked by 2-amino-5-phosphonovalerate (APV, 50 µM). The fast component of Type 1 EPSCs had a linear current-voltage relationship and reversed at a membrane potential of 7.6 ± 1.3 mV (n = 5). The fast component of Type 2 EPSCs was also blocked by 5 µM CNQX and the remaining slower component was blocked by 50 µM APV. When the DCM was stimulated in the presence of 50 µM APV, the time to peak and decay time constant in Type 1 EPSCs were 1.9 ± 0.2 and 4.1 ± 0.8 ms, respectively. Examination of the NMDA receptor-mediated component of the EPSCs in the presence of 5 µM CNQX revealed a current-voltage relationship that had a region of negative slope conductance (from 20 to 80 mV), which was abolished in Mg²⁺-free external solution. The time to peak and decay time constant of this component were 14.2 ± 2.0 and 91.0 ± 12.4 ms, respectively. Type 1 EPSCs in some PGN responded in an all-or-none manner and presumably represented unitary synaptic responses; whereas Type 2 EPSCs always exhibited a graded stimulus intensity-response relationship. Paired-pulse facilitation (50-ms interstimulus intervals; 141 ± 5.6% increase, n = 8) of EPSCs was observed. These results indicate that PGN receive monosynaptic and polysynaptic glutamatergic excitatory inputs from neurons and/or axonal pathways in the DCM.