Presynaptic inhibition of sensory neurons during kicking movements in the locust.
1. Locusts use a distinctive motor pattern to extend the tibia of a hind leg rapidly in a defensive kick, or to extend the tibiae of both hind legs in a jump. The force for the movement is generated by an almost isometric co-contraction of the extensor and flexor tibiae muscles followed by a sudden release of the stored energy when the flexor motor neurons are inhibited. A proprioceptor (the femoral chordotonal organ) spans the femorotibial joint, and at least 50 of its sensory neurons each signal particular features of its movements. Intracellular recordings from these neurons close to their terminals in the CNS show that their spikes during kicking are superimposed on a depolarizing synaptic input generated near their output terminals. The depolarization is linked to the time in the motor pattern when the sensory neurons spike. 2. Flexion-sensitive neurons spike and their terminals are depolarized when the tibia is initially flexed and when the tibia rebounds from the rapid extension of the kick. Some respond phasically, others more tonically and over different ranges of joint angles, but all receive a depolarizing synaptic input when they spike. The depolarization of the terminals precedes the spikes and often occurs concurrently with the changes in the membrane potentials of the motor neurons. The input persists while the tibia is held fully flexed before the kick. 3. Extension-sensitive neurons spike and their terminals are depolarized when the tibia is rapidly extended and this depolarization may outlast the spikes at the completion of a kick. Some of these depolarizing synaptic potentials occur before the movement starts, which suggests that they may result from central elements of the motor pattern; others however are clearly consequent upon joint movements. During the co-contraction that precedes the movement, these neurons do not spike and their membrane potential repolarizes because of a reduction in the synaptic input. 4. The depolarizing synaptic potentials are associated with a fall in the resistance of the membrane and may be attributed to the same gamma-aminobutyric acid-mediated mechanism already identified at the terminals of these sensory neurons. The effect and timing of the depolarization of the terminals during this voluntary movement should be to reduce the effectiveness of the sensory neurons in transmitting signals to their postsynaptic neurons in the CNS. This could therefore be part of a mechanism that allows voluntary movements to proceed in the presence of self-generated sensory feedback which might otherwise impede that movement.
Hedwig
B
B
Department of Zoology, University of Cambridge, United Kingdom.
Burrows
M
M
D000818:Animals; D017950:Ganglia, Sensory / Q000502:physiology*; D006110:Grasshoppers; D008564:Membrane Potentials / Q000502:physiology; D009068:Movement / Q000502:physiology*; D009474:Neurons / Q000502:physiology*; D009435:Synaptic Transmission / Q000502:physiology*; D013977:Tibia / Q000502:physiology