D. Le Ray et D. Cattaert, Active motor neurons potentiate their own sensory inputs via glutamate-induced long-term potentiation, J NEUROSC, 19(4), 1999, pp. 1473-1483
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.