Neural circuits in the flight system of the locust

Abstract

Circuitry in the flight system of the locust, Locusta migratoria, was investigated by use of intracellular recording and staining techniques. Neuronal connections were established by recording simultaneously from neuropile segments of pairs of identified interneurons. Brief depolarizing current pulses delivered to interneurons 301 and 501 reset the flight rhythm in a phase-dependent manner, thus establishing the importance of these neurons in rhythm generation. Interneuron 301 was found to make a strong delayed excitatory connection with 501 and to receive a short-latency inhibitory connection from 501. The circuit formed by 301 and 501 appears suited for promoting rhythmicity in the flight system. The delayed excitatory potential recorded in 501 following each spike of 301 was reversed by hyperpolarizing 501. This potential and short-latency inhibitory postsynaptic potentials from 301 to other interneurons were blocked with the application of picrotoxin. We conclude that the delayed excitation is produced via a disynaptic pathway from 301 to 501, with 301 inhibiting in a graded manner the tonic release of transmitter from one or more unidentified intercalated neurons. Interconnections between the 301-501 circuit and other identified interneurons were discovered. This circuitry can account for two features of the flight motor pattern recorded in deafferented preparations. These features are the constant-latency relationship between depolarizations in elevator and depressor motoneurons and the relatively constant duration of depressor motoneuron bursts. The locust flight system shares general features with other described rhythm-generating systems. These include the occurrence of graded interactions, the probability of multiple oscillatory mechanisms, and a predominance of inhibitory connections. Its uniqueness lies in the way that components and processes are assembled and operate.