Active motor neurons potentiate their own sensory inputs via glutamate-induced long-term potentiation

Adaptive motor control is based mainly on the processing and integration of proprioceptive feedback information. In crayfish walking leg, many of thes e operations are performed directly by the motor neurons (MNs), which are c onnected monosynaptically by sensory afferents (CBTs) originating from a ch ordotonal organ that encodes vertical limb movements. An in vitro preparati on of the crayfish CNS was used to investigate a new control mechanism exer ted directly by motor neurons on the sensory inputs themselves. Paired intr acellular recordings demonstrated that, in the absence of any presynaptic s ensory firing, the spiking activity of a leg MN is able long-lastingly to e nhance the efficacy of the CBT-MN synapses. Moreover, this effect is specif ic to the activated MN because no changes were induced at the afferent syna pses of a neighboring silent MN. We report evidence that long-term potentia tion (LTP) of the monosynaptic EPSP involves a retrograde system of glutama te transmission from the postsynaptic MN, which induces the activation of a metabotropic glutamate receptor located presynaptically on the CBTs. We de monstrate that LTP at crayfish sensory-motor synapses results exclusively f rom the long-lasting enhancement of release of acetylcholine from presynapt ic sensory afferent terminals, without inducing any modifications in postsy naptic MN properties. Our data indicate that this positive feedback control represents a functional mechanism that may play a key role in the auto-org anization of sensory-motor networks.