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Journal of Neuroscience, Vol 15, 6035-6045, Copyright © 1995 by Society for Neuroscience
Intrinsic neuromodulation in the Tritonia swim CPG: the serotonergic dorsal swim interneurons act presynaptically to enhance transmitter release from interneuron C2
PS Katz and WN Frost
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston 77030, USA.
Heterosynaptic enhancement of transmitter release is potentially very
important for neuronal computation, yet, to our knowledge, no prior study
has shown that stimulation of one neuron directly enhances release from an
interneuron. Here, we demonstrate that in the marine mollusk Tritonia
diomedea, the serotonergic dorsal swim interneurons (DSIs)
heterosynaptically increase the amount of transmitter released from another
interneuron, C2. Stimulation of a single DSI at physiological firing
frequencies increases the size of synaptic potentials evoked by C2. This
increase in synaptic efficacy is correlated with an increase in
homosynaptic paired-pulse facilitation by C2. Thus, it is likely to be due
to an enhancement of transmitter release from C2, rather than a
postsynaptic action on the followers of C2. This is further supported by
the fact that DSI stimulation enhances the strengths of all chemical
synapses made by C2 within the swim network, regardless of their sign.
Furthermore, DSI enhances the amplitude of C2 synaptic potentials recorded
in neurons that DSI itself does not synapse with. Finally, DSI
differentially modulates different synaptic inputs to the same postsynaptic
target; while increasing C2- evoked EPSPs it simultaneously decreases the
size of EPSPs evoked by other DSIs. The heterosynaptic facilitation of C2
synaptic potentials by DSI is not caused by a simple depolarization of C2,
but may be a direct action on the transmitter release mechanism. This
neuromodulatory effect, which is intrinsic to the circuitry of the central
pattern generator for escape swimming in Tritonia, may be important for
self-reconfiguration of the swim motor network.
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