Local circuits underlying excitation and inhibition of intersegmental interneurones in the locust

Abstract

1. A population of some 30 paired identifiable intersegmental interneurones in the locustSchistocerca gregaria receive inputs from mechanoreceptors on one middle leg and transmit this information to the local circuits controlling the ipsilateral hindleg. The integrative processes shaping the receptive fields of these neurones were revealed by extracellular recordings from middle leg afferents and intracellular recordings from spiking local interneurones and the intersegmental interneurones in the mesothoracic ganglion. 2. An intersegmental interneurone can have excitatory and inhibitory regions to its receptive field, being excited by exteroceptors on one region of the middle leg ipsilateral to its arborizations, and inhibited by others on different regions of the same leg. Within the population, the interneurones differ in the sizes and shapes of their receptive fields (Fig. 1 and Table 1). 3. The excitatory region of a receptive field is formed by direct inputs from the sensory afferents. Spikes of hair afferents evoke excitatory postsynaptic potentials (EPSPs) that summate and give rise to spikes in the intersegmental interneurones. The central delay between the afferent spikes and the EPSPs is 1 to 2 ms. The afferents also evoke EPSPs with the same latency in a population of spiking local interneurones with cell bodies at the ventral midline of the ganglion. The branches of the sensory afferents and the interneurones overlap in the neuropil (Figs. 2, 3, 4). 4. The inhibitory region of a receptive field is formed by inputs from the spiking local interneurones. Spikes in particular spiking local interneurones that result from mechanical stimulation of exteroceptors on the leg, or from intracellular injection of current, lead to inhibitory postsynaptic potentials (IPSPs) in particular intersegmental interneurones after a constant delay of 1.0±0.2 ms. This inhibitory relationship is unidirectional (Fig 5). 5. The output of 75% of these intersegmental interneurones is determined by a summation of inputs from different regions and/or joints of the leg. For example, the excitation caused by movement of a joint can be gated if strain is provided simultaneously to the leg. Because each of these stimuli corresponds only to a certain phase of the step cycle, the signals delivered by these interneurones during walking could thus represent key features of the on-going leg movement and position (Figs. 6–9).