The Journal of Neuroscience, February 15, 1999, 19(4):1473-1483
Active Motor Neurons Potentiate Their Own Sensory Inputs via
Glutamate-Induced Long-Term Potentiation
Didier
Le Ray and
Daniel
Cattaert
Laboratoire Neurobiologie et Mouvements, Centre National de la
Recherche Scientifique, 13402 Marseille, Cedex 20, France
Adaptive motor control is based mainly on the processing and
integration of proprioceptive feedback information. In crayfish walking
leg, many of these operations are performed directly by the motor
neurons (MNs), which are connected monosynaptically by sensory
afferents (CBTs) originating from a chordotonal organ that encodes
vertical limb movements. An in vitro preparation of the
crayfish CNS was used to investigate a new control mechanism exerted
directly by motor neurons on the sensory inputs themselves. Paired
intracellular recordings demonstrated that, in the absence of any
presynaptic sensory firing, the spiking activity of a leg MN is able
long-lastingly to enhance the efficacy of the CBT-MN synapses.
Moreover, this effect is specific to the activated MN because no
changes were induced at the afferent synapses of a neighboring silent
MN. We report evidence that long-term potentiation (LTP) of the
monosynaptic EPSP involves a retrograde system of glutamate
transmission from the postsynaptic MN, which induces the activation of
a metabotropic glutamate receptor located presynaptically on the CBTs.
We demonstrate that LTP at crayfish sensory-motor synapses results
exclusively from the long-lasting enhancement of release of
acetylcholine from presynaptic sensory afferent terminals, without
inducing any modifications in postsynaptic MN properties. Our data
indicate that this positive feedback control represents a functional
mechanism that may play a key role in the auto-organization of
sensory-motor networks.
Key words:
glutamate; long-term potentiation; EPSP; crayfish; sensory-motor synapse; metabotropic glutamate receptor; quantal
analysis
Copyright © 1999 Society for Neuroscience 0270-6474/99/1941473-11$05.00/0
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