Disynaptic and polysynaptic statocyst pathways to an identified set of premotor nonspiking interneurons in the...

Nonspiking giant interneurons (NGIs) in the crayfish brain occupy a key position in the neuronal circuit for eyestalk motor control and, hence, play a crucial role in the central compensation process following unilateral deprivation of the statocyst that functions as an equilibrium sensory system. The synaptic organization of their input pathways, however, remains unknown. In the present study we identified 11 local interneurons that were polysynaptically connected to NGIs by making simultaneous intracellular recordings. We also identified three other local interneurons that connected to NGIs monosynaptically. PLNI-2 was a nonspiking interneuron making an excitatory synaptic connection to an NGI that had its cell body on the opposite side. PLSI was a spiking interneuron that made an inhibitory connection to an ipsilateral NGI. These cells were entirely confined to the protocerebrum. Another local spiking interneuron termed UGLI-1 was found to make an excitatory connection with a contralateral NGI, extending dendrites in the anterior and posterior medial protocerebral neuropils and the lateral antenna I neuropil in the deutocerebrum where statocyst afferents project. When a depolarizing current was injected into the UGLI-1, the frequency of discrete excitatory PSPs increased remarkably in the postsynaptic NGI, each PSP following the UGLI-1 spike in one-to-one correspondence. The UGLI was previously reported to be activated monosynaptically by statocyst afferents. The present study thus finally demonstrates the tri-synaptic organization of the statocyst-to-eyestalk motor neuron pathway in its simplest form, suggesting the critical role of the UGLI-1 in the central compensation.