Nonspiking interneurons

The non-spiking interneurons (Fig. 8.7a) provide a major source of input to leg motor neurons. As their name suggests, these interneurons do not spike when they are excited, but changes in membrane potential directly affect the rate at which neurotransmitter is released from their output synapses. There is a smoothly graded relationship between the membrane potential of a non-spiking interneuron and of a motor neuron that it drives (Burrows & Siegler, 1978), which is seen when one electrode is used to inject current into a non-spiking interneuron while another one is used to record the membrane potential of a postsynaptic motor neuron. The same relationship between presynaptic and postsynaptic potentials is found at all chemical synapses, but the all-or-nothing nature of a spike often obscures it. In the recordings shown in Fig. 8.7b, recordings were made from two different motor neurons at the same time. The interneuron inhibited the flexor

Figure 8.7 Non-spiking interneurons in the third thoracic ganglion of a locust. (a) The morphology of a non-spiking interneuron that excites the slow extensor tibiae motor neuron. (b) Intracellular recordings that show the graded nature of transmission from a non-spiking interneuron. One electrode was used to inject pulses of depolarising current into an interneuron, while a second electrode recorded the intracellular potential of a motor neuron of a leg extensor muscle, and a third electrode recorded from a motor neuron of a leg flexor muscle. When the strength of current increased, the potential changes in the two motor neurons also increased. As the circuit on the right indicates, the non-spiking interneuron probably made a direct, inhibitory connection with the flexor motor neuron, and excited the extensor motor neuron by reducing tonic inhibition from another non-spiking interneuron. (a from Watkins, Burrows & Siegler, 1985; reprinted by permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons Inc.; b modified after Burrows, 1989.)

Figure 8.7 Non-spiking interneurons in the third thoracic ganglion of a locust. (a) The morphology of a non-spiking interneuron that excites the slow extensor tibiae motor neuron. (b) Intracellular recordings that show the graded nature of transmission from a non-spiking interneuron. One electrode was used to inject pulses of depolarising current into an interneuron, while a second electrode recorded the intracellular potential of a motor neuron of a leg extensor muscle, and a third electrode recorded from a motor neuron of a leg flexor muscle. When the strength of current increased, the potential changes in the two motor neurons also increased. As the circuit on the right indicates, the non-spiking interneuron probably made a direct, inhibitory connection with the flexor motor neuron, and excited the extensor motor neuron by reducing tonic inhibition from another non-spiking interneuron. (a from Watkins, Burrows & Siegler, 1985; reprinted by permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons Inc.; b modified after Burrows, 1989.)

motor neuron and excited the extensor, probably by disinhibition of a second, inhibitory non-spiking interneuron (cf. section 7.6).

Many of the non-spiking interneurons release neurotransmitter toni-cally, exerting a steady synaptic drive on their postsynaptic targets. One important result is that they regulate the passage of sensory information to motor neurons, illustrated as follows for a pathway in which a sensory neuron excites a non-spiking interneuron which, in turn, excites a motor neuron. If the non-spiking interneuron is relatively hyperpolarised as a result of a particular combination of sensory inputs, its membrane potential will be below the threshold for transmitter release and its output synapses will effectively be switched off. As a result, exciting the sensory neuron to produce a spike will cause an EPSP in the interneuron, but this will be too small to cause the interneuron to release neurotransmitter and excite the motor neuron. If the angle of the joint is altered, the new combination of sensory inputs onto the interneuron might excite it sufficiently for it to release transmitter tonically, which will excite the motor neuron with a steady, depolarising potential. Now if the sensory receptor is excited, the EPSP it causes in the interneuron will be passed on to the motor neuron (Burrows, 1979). The non-spiking interneurons, therefore, can act as summing points, where signals including those from proprioceptors, tactile sense organs, and interneurons that co-ordinate activity between different segments are integrated before being passed on to the motor neurons. The result is that local reflex movements are modulated according to behavioural context. Interestingly, when the angle of a joint changes, the size of the change in membrane potential that occurs in non-spiking interneurons depends on whether the joint angle has increased or decreased (Siegler, 1981). This means that the properties of the interneuron and its output synapses depend upon the recent history of movements the locust has made.

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