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Journal of Neuroscience, Vol 14, 2636-2647, Copyright © 1994 by Society for Neuroscience
Presynaptic inhibition of primary afferent transmitter release by 5- hydroxytryptamine at a mechanosensory synapse in the vertebrate spinal cord
KT Sillar and AJ Simmers
Gatty Marine Laboratory, School of Biological and Medical Sciences, University of St. Andrews, Fife, Scotland.
The effects of the neuromodulatory monoamine 5-HT (serotonin) on a
cutaneous mechanosensory (Rohon-Beard, R-B neuron) pathway in the spinal
cord of postembryonic Xenopus laevis tadpoles have been examined. In
paralyzed animals, exogenous 5-HT at 1-10 microM reversibly inhibits
(within 1-2 min) the activation of fictive swimming in response to
electrical stimulation of R-B free nerve endings in the skin. At threshold
stimulus intensities for swimming under control conditions, intracellularly
recorded EPSPs in contralateral motoneurons are completely abolished by
5-HT without any obvious change in neuronal conductance or membrane
potential. However, increasing the stimulus voltage can activate swimming
with enhanced motor burst discharge on each cycle (Sillar et al., 1992).
This suggested that 5-HT inhibits the swim-initiating pathway rather than
the motor rhythm-generating circuitry itself. Extracellular recordings from
the central projections of R-B neurons indicated that the amine does not
impair the generation of mechanoafferent impulses or their propagation into
the spinal cord. However, 5-HT application blocks impulse activity in
dorsolaterally positioned sensory interneurons (DLis) that are contacted by
R-B neurons, suggesting that 5-HT acts at R-B to DLi synapses in the dorsal
cord. By recording with microelectrodes from DLis, we find that skin
stimulus-evoked EPSPs at this first-order synapse in the swim- initiating
pathway are reversibly suppressed by 5-HT. No obvious change in DLi
membrane potential or conductance could be detected during the inhibition,
suggesting a presynaptic site of action for 5-HT. To investigate this
suggestion further, the effects of 5-HT on the spontaneous release of R-B
sensory transmitter (excitatory amino acid, EAA) were examined, again by
recording postsynaptically from DLis. In quiescent preparations, DLis
receive spontaneous glycinergic, GABAergic, and EAA receptor-mediated PSPs.
The inhibitory potentials are abolished by strychnine and curare,
respectively. The excitatory potentials that remain are not blocked by
application of the calcium channel blocker cadmium chloride at 1 mM, but
are suppressed by the EAA receptor antagonist kynurenic acid. They
therefore resemble the TTX- resistant EPSPs described previously in Xenopus
DLis (Sillar and Roberts, 1991), which are presumed to arise from the
spontaneous liberation of EAA transmitter from R-B terminals. Bath
application of 5- HT dramatically reduces the rate of occurrence of these
spontaneous EPSPs consistent with a presynaptic locus for the inhibitory
effects of 5-HT.(ABSTRACT TRUNCATED AT 400 WORDS)
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