Synaptic responses of substantia gelatinosa neurones to dorsal column stimulation in rat spinal cord in vitro.

Abstract

1. To study the mechanism of dorsal column stimulation-induced depression of nociceptive transmission in the spinal cord, synaptic responses evoked in dorsal horn neurones by dorsal column and dorsal root stimulations were examined in a horizontal spinal cord slice of the adult rat. Intracellular recordings were made from substantia gelatinosa (SG) neurones. 2. All SG neurones examined received monosynaptic inputs and/or polysynaptic inputs from both dorsal column and dorsal root. Ad fibres were probably responsible for the synaptic responses. The responses evoked by dorsal column stimulation were similar to those evoked by primary afferent Ad fibre stimulation. 3. Monosynaptic excitatory postsynaptic potentials (EPSPs) evoked by dorsal column Ad fibres were depressed by 6-cyano-7-nitroquinoxaline-2,3-dione, suggesting that these fibres released L-glutamate or a related amino acid as a transmitter. 4. In 38 of 101 SG neurones, dorsal column stimulation evoked an initial EPSP followed by fast and/or slow inhibitory postsynaptic potentials (IPSPs). These IPSPs reversed polarity at a membrane potential of -73 + 2 mV. The fast IPSPs observed in 16 of the SG neurones (42 %) that received inhibitory inputs were depressed by strychnine, while the slow IPSPs observed in 22 SG neurones were depressed by bicuculline. In a few cells, a long-lasting slow IPSP with a much slower time course was detected; this IPSP was insensitive to strychnine and bicuculline, and reversed polarity at a membrane potential near -90 mV. 5. Repetitive stimulation of the dorsal column depressed the amplitude of monosynaptic EPSPs evoked by dorsal root stimulation. 6. The responses of SG neurones to dorsal column stimulation had configurations and durations similar to responses to dorsal root stimulation, and may be mediated largely by the same Ad fibres. However, a C fibre-mediated response could not be detected in SG neurones from dorsal column stimulation, although dorsal root stimulation could evoke C fibre-mediated monosynaptic EPSPs in 18 of 88 SG neurones (20 %). 7. These observations suggest that SG neurones receive abundant AS but not C fibre inputs from the dorsal column and that dorsal column stimulation inhibits primary afferent transmission in the spinal cord both by reducing transmitter release from primary Ad fibres and by hyperpolarizing SG neurones.Many fine afferent fibres that carry nociceptive information fibre classes and to modify the output of projection neurones terminate in the superficial dorsal horn of the spinal cord, located in lamina I and in deeper regions of the dorsal horn particularly in the substantia gelatinosa (SG, lamina II of (Kumazawa & Perl, 1978;Light, Trevino & Perl, 1979). Rexed) (Rexed, 1952;Maxwell & Rethelyi, 1987; Sugiura, Melzack & Wall (1965) proposed the gate control theory for Terui & Hosoya, 1989;Yoshimura & Jessell, 1989a. the dorsal horn circuitry responsible for pain transmission. SG neurones form local interneuronal circuits that are In their model, SG inhibitory neurones, activated by la...

Primary afferent‐evoked glycine‐ and GABA‐mediated IPSPs in substantia gelatinosa neurones in the rat spinal cord in vitro.

“…Analysis of the IPSPs in the SG at the single cell level, however, has been hampered mainly due to the difficulty of obtaining stable intracellular recordings in in vivo experiments. We have developed an in vitro slice preparation which retains an attached dorsal root, cut from the adult rat spinal cord (Yoshimura & Jessell, 1989, 1990Yoshimura & Nishi, 1993;Baba et al 1994). In the present study, we report that the stimulation of primary afferent Ad fibres evokes two different types of IPSPs (short and long IPSPs) in substantia gelatinosa neurones and that the short and long IPSPs are mediated by strychnine-and bicuculline-sensitive receptors, respectively.…”

“…The methods used for obtaining slice preparations of adult rat spinal cord were similar to those described elsewhere (Yoshimura & Nishi, 1993;Baba et al 1994). Briefly, male Sprague-Dawley rats (6-12 weeks old) were anaesthetized with urethane (1'2 g kg-', i.p.)…”

“…The present pharmacological results further support this idea. In addition to these relatively short-lasting IPSPs, a longlasting IPSP, which has a much slower time course ranging from 1 to 30 s, has been reported in the horizontal slice following the Ad fibre stimulation (Baba et al 1994). Longlasting IPSPs were also observed in the transverse slices but appear to be less frequent, probably due to impairment pharmacological nature of long-lasting IPSPs was not analysed further in the present study.…”

“…This shows that both IPSPs and EPSP are evoked by afferents in the same threshold range. Stimulation of Ad fibres in the dorsal column has also been shown to evoke glycinergic and GABAergic IPSPs in SG neurones (Baba et al 1994). Based on their physiological properties, it is suggested that the short and long IPSPs evoked by dorsal column stimulation are the result of activating axon collaterals of afferent Ad fibres.…”

Mechanisms for the Anti-nociceptive Actions of the Descending Noradrenergic and Serotonergic Systems in the Spinal Cord

“…Fine myelinated Aδ and unmyelinated C primary afferent fibers, many of which innervate nociceptors, tend to terminate preferentially on the neurons of the superficial dorsal horn, particularly the SG neurons (21 -29). Intracellular recording studies of the SG neurons have also revealed that the stimulation of primary afferent evokes monosynaptic fast excitatory postsynaptic potentials (EPSPs) and inhibitory postsynaptic potentials (IPSPs) in the majority of SG neurons (30,31). In addition, in vivo patch-clamp recording studies have shown that the majority of SG neurons are excited by noxious stimuli (21,22).…”