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The Journal of Neuroscience, October 1, 1998, 18(19):8095-8110

Cellular and Synaptic Modulation Underlying Substance P-Mediated Plasticity of the Lamprey Locomotor Network

David Parker and Sten Grillner

Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institute, S-17177, Stockholm, Sweden

The tachykinin substance P modulates the lamprey locomotor network by increasing the frequency of NMDA-evoked ventral root bursts and by making the burst activity more regular. These effects can last in excess of 24 hr. In this paper, the effects of substance P on the synaptic and cellular properties of motor neurons and identified network interneurons have been examined.

Substance P potentiated the amplitude of monosynaptic glutamatergic inputs from excitatory interneurons and reticulospinal axons. The amplitude and frequency of miniature EPSPs was increased, suggesting that the synaptic modulation was mediated presynaptically and postsynaptically. The postsynaptic modulation was caused by a specific effect of substance P on the NMDA component of the synaptic input, whereas the presynaptic component was calcium-independent. Substance P did not affect monosynaptic glycinergic inputs from lateral interneurons, crossed inhibitory interneurons, or ipsilateral segmental interneurons or postsynaptic GABA_A or GABA_B responses, suggesting that it has little effect on inhibitory synaptic transmission.

At the cellular level, substance P increased synaptic inputs, resulting in membrane potential oscillations in motor neurons, crossed caudal interneurons, lateral interneurons, and excitatory interneurons. The spiking in response to depolarizing current pulses was increased in motor neurons, lateral interneurons, and excitatory interneurons, but usually was reduced in crossed inhibitory interneurons. Substance P reduced the calcium-dependent afterhyperpolarization after an action potential in motor neurons and lateral interneurons, but did not affect this conductance in excitatory or crossed inhibitory interneurons.

The relevance of these cellular and synaptic changes to the modulation of the locomotor network is discussed.

Key words: substance P; neuropeptide; neuromodulation; lamprey; synaptic transmission; synaptic plasticity

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Copyright © 1998 Society for Neuroscience  0270-6474/98/18198095-16$05.00/0

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