Abstract
Walking and flying in locusts are exemplary rhythmical behaviors generated by central pattern generators (CPG) that are tuned in intact animals by phasic sensory inputs. Although these two behaviors are mutually exclusive and controlled by independent CPGs, leg movements during flight can be coupled to the flight rhythm. To investigate potential central coupling between the underlying CPGs, we used the muscarinic agonist pilocarpine and the amines octopamine and tyramine to initiate fictive flight and walking in deafferented locust preparations. Our data illustrate that fictive walking is readily evoked by comparatively lower concentrations of pilocarpine, whereas higher concentrations are required to elicit fictive flight. Interestingly, fictive flight did not suppress fictive walking so that the two patterns were produced simultaneously. Frequently, leg motor units were temporally coupled to the flight rhythm, so that each spike in a step cycle volley occurred synchronously with wing motor units firing at flight rhythm frequency. Similarly, tyramine also induced fictive walking and flight, but mostly without any coupling between the two rhythms. Octopamine in contrast readily evoked fictive flight but generally failed to elicit fictive walking. Despite this, numerous leg motor units were recruited, whereby each was temporarily coupled to the flight rhythm. Our results support the notion that the CPGs for walking and flight are largely independent, but that coupling can be entrained by aminergic modulation. We speculate that octopamine biases the whole motor machinery of a locust to flight whereas tyramine primarily promotes walking.
Highlights
Central pattern generators (CPG) are the basis of many ongoing repetitive movements and have been intensively studied on the cellular and network levels over the past two decades
Natural walking in intact freely behaving locusts is characterized by a burst of swing phase motor units, followed after a delay by a longer burst of stance phase units, whereby the swing phase is the shorter and occupies about 20% of a step cycle (Fig. 2A), which varies in intact animals from 200–1300 ms [34]
For tethered flight of intact locusts, individual motor units are usually activated only once or twice per cycle, whereby the wing elevator and wing depressor units fire in alternation and the WD-WE latency is generally 55% of the total cycle length (Fig. 2B) which lasts some 50 ms, but 80 or more ms in deafferented preparations [35]
Summary
Central pattern generators (CPG) are the basis of many ongoing repetitive movements and have been intensively studied on the cellular and network levels over the past two decades (reviews: [13]). The most influential finding emergent from work on CPGs is that each synapse in a network is a target to modulation by a wide variety of neuromodulators This astonishing plasticity has led to the realization that an anatomically defined neuronal circuit has the potential to generate a wide variety of outputs, by modulating the degree of synaptic coupling between its individual elements. For example, the respiratory rhythm becomes reconfigured [13] and leg movements may be coupled to the wing-beat cycle [14] Such effects could result from afferent control since in intact animals proprioceptive feedback plays an important role in tuning CPGs to generate functionally adequate motor activity [15]. In this paper we aim to reveal central interactions between the flight and walking CPGs of the locust Schistocerca gregaria by using aminergic and cholinergic agonists to elicit fictive motor patterns in deafferented preparations in which all sources of potential sensory feedback are eliminated
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