The locust frontal ganglion: a central pattern generator network controlling foregut rhythmic motor patterns (original) (raw)
Related papers
Interactions of suboesophageal ganglion and frontal ganglion motor patterns in the locust
Journal of Insect Physiology, 2008
Although locust feeding has been well studied, our understanding of the neural basis of feeding-related motor patterns is still far from complete. This paper focuses on interactions between the pattern of rhythmic movements of the mouth appendages, governed by the suboesophageal ganglion (SOG), and the foregut movements, controlled by the frontal ganglion (FG), in the desert locust. In vitro simultaneous extracellular nerve recordings were made from totally isolated ganglia as well as from fully interconnected SOG-FG and brain-SOG-FG preparations. SOG-confined bath application of the nitric oxide donor, SNP, or the phosphodiesterase antagonist, IBMX, each followed by the muscarinic agonist pilocarpine, consistently induced robust fictive motor patterns in the SOG. This was observed in both isolated and interconnected preparations. In the brain-SOG-FG configuration the SOG-confined modulator application had an indirect excitatory effect on spontaneous FG rhythmic activity. Correlation between fictive motor patterns of the two ganglia was demonstrated by simultaneous changes in burst frequency. These interactions were found to be brain-mediated. Our results indicate the presence of intricate neuromodulation-mediated circuit interactions, even in the absence of sensory inputs. These interactions may be instrumental in generating the complex rhythmic motor patterns of the mandibles and gut muscles during locust feeding or ecdysis-related air swallowing.
The role of the frontal ganglion in locust feeding and moulting related behaviours
The Journal of experimental biology, 2002
In the desert locust, Schistocerca gregaria, the frontal ganglion (FG) plays a key role in control of foregut movements, and constitutes a source of innervation to the foregut dilator muscles. In this work we studied the generation and characteristics of FG motor outputs in two distinct and fundamental behaviours: feeding and moulting. The FG motor pattern was found to be complex, and strongly dependent on the locust's physiological and behavioural state. Rhythmic activity of the foregut was dependent on the amount of food present in the crop; animals with food in their crop demonstrated higher FG burst frequency than those with empty crop. A very full gut inhibited the FG rhythm altogether. When no feeding-related foregut pattern was observed, the FG motor output was strongly correlated with the locust's ventilation pattern. This ventilation-related rhythm was dominant in pre-moulting locusts. During the moult, synchronization with the ventilation pattern can be transiently...
Neuromodulation for behavior in the locust frontal ganglion
Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, 2004
Neuromodulators orchestrate complex behavioral routines by their multiple and combined effects on the nervous system. In the desert locust, Schistocerca gregaria, frontal ganglion neurons innervate foregut dilator muscles and play a key role in the control of foregut motor patterns. To further investigate the role of the frontal ganglion in locust behavior, we currently focus on the frontal ganglion central pattern generator as a target for neuromodulation. Application of octopamine, a well-studied insect neuromodulator, generated reversible disruption of frontal ganglion rhythmic activity. The threshold for the modulatory effects of octopamine was 10 )6 mol l )1 , and 10 )4 mol l )1 always abolished the ongoing rhythm. In contrast to this straightforward modulation, allatostatin, previously reported to be a myoinhibitor of insect gut muscles, showed complex, tri-modal, dose-dependent effects on frontal ganglion rhythmic pattern. Using a novel cross-correlation analysis technique, we show that different allatostatin concentrations have very different effects not only on cycle period but also on temporal characteristics of the rhythmic bursts of action potentials. Allatostatin also altered the frontal ganglion rhythm in vivo. The analysis technique we introduce may be instrumental in the study of not fully characterized neural circuits and their modulation. The physiological significance of our results and the role of the modulators in locust behavior are discussed.
The Insect Frontal Ganglion and Stomatogastric Pattern Generator Networks
Neurosignals, 2004
Insect neural networks have been widely and successfully employed as model systems in the study of the neural basis of behavior. The insect frontal ganglion is a principal part of the stomatogastric nervous system and is found in most insect orders. The frontal ganglion constitutes a major source of innervation to foregut muscles and plays a key role in the control of foregut movements.
Interactions among different neuronal circuits are essential for adaptable coordinated behavior. Specifically, higher motor centers and central pattern generators (CPGs) induce rhythmic leg movements that act in concert in the control of locomotion. Here we explored the relations between the subesophageal ganglion (SEG) and thoracic leg CPGs in the desert locust. Backfill staining revealed about 300 SEG descending interneurons (DINs) and some overlap with the arborization of DINs and leg motor neurons. In accordance, in in-vitro preparations, electrical stimulation applied to the SEG excited these neurons, and in some cases also induced CPGs activity. Additionally, we found that the SEG regulates the coupling pattern among the CPGs: when the CPGs were activated pharmacologically, inputs from the SEG were able to synchronize contralateral CPGs. This motor output was correlated to the firing of SEG descending and local interneurons. Altogether, these findings point to a role of the SE...
Rhythmic behaviour and pattern-generating circuits in the locust: Key concepts and recent updates
Journal of Insect Physiology, 2010
The insect nervous system has been widely and successfully employed as a model system in the study of the neural basis of behaviour (Hoyle, 1975; Burrows, 1996; Bä ssler and Bü schges, 1998). The locust, traditionally studied for various practical, historical, sociological and economic reasons, has provided an important insect neurophysiological preparation, offering a very well defined nervous system with identifiable neurons (Burrows, 1996). In studying the neural basis of behaviour, there is a great advantage in choosing ongoing and repetitive movements, i.e. rhythmic behavioural patterns. These include fundamental and vital behaviours for all animals, such as breathing, chewing, walking, flying, oviposition, and more. One common feature of practically all rhythmic patterns studied to date is that they are generated and controlled by discrete neural circuits in the animal's central nervous system (CNS), referred to as central pattern generators (CPGs)
Journal of Insect Physiology, 1984
Lesion and stimulation experiments suggest that the suboesophageal ganglion (SOG) plays a special role in the control of insect behaviour: in bilateral coordination and by maintaining ongoing motor activity. Anatomical observations indicate that there are descending interneurones (DINS) originating in the SOG in addition to those from the brain. An SOG preparation for sampling both types of DIN intracellularly in walking locusts is described. Forty-three units showing activity changes during leg movements and walking were recorded. Using dye injection six were shown to be through-running axons; one was an SOG ascending interneurone; and eight were SOG DINS. 7 contralateral, one ipsilateral. All fired before or during movements and received various sensory inputs. Many gave complex responses to different modalities, several showing directional preferences. Some SOG neurones showed spontaneous changes in activity; activity outlasting movements; or responses to passive as well as active movements. These preliminary results suggest neuronal substrates for the special functions of the SOG in behaviour. They also indicate that DINS, rather than being simple relays, are part of a dynamic network which includes the motor centres. Regulation of complex and subtle aspects of behaviour may be achieved by dynamic and sequential patterns of activity in groups of DINS, some of which may be multifunctional.
Journal of Insect Physiology, 1996
The control of a motor pattern generator in the VIIth abdominal ganglion of Locusta was examined. Sucrose gap block of ventral nerve cord neural activity in non-egg-laying locusts, anterior to the VIIth abdominal ganglion, initiated the rhythmic neural activity in the oviducal nerves which is produced by this motor pattern generator. Removal of the sucrose gap block resulted in the cessation of the pattern. Extracellular stimulation of the nerve cord caused the inhibition of the rhythmic neural activity in preparations in which the pattern was initiated by transection of the ventral nerve cord. Taken together, these results confirm that the main control of the central pattern generator in the VIIth abdominal ganglion is by descending neural inhibition. Using serial transections of the ventral nerve cord, the source of the inhibition was localized to the brain, suboesophageal ganglion and thoracic ganglia. In addition to being controlled by descending neural inhibition, the motor pattern generator in the VIIth abdominal ganglion was also found to be coordinated with the oviposition digging central pattern generator in the VIIIth abdominal ganglion. The data suggest that communication with the digging central pattern generator may be important in view of the fact that the outputs of these distinct pattern generators are highly coordinated.
Spontaneous behavioral rhythms in the isolated CNS of insects – Presenting new model systems
Journal of Physiology-Paris, 2013
Three new model systems for the study of rhythm generation in the isolated insect central nervous system are presented. Natural behavioral rhythms are produced in these cases spontaneously in the isolated CNS. They can be monitored as output of motoneurons at peripheral nerves. Recording from the neurons of the pattern generating networks during this output gives insight into neural control principles of locust respiration, of hemolymph pumping in accessory pumping organs of crickets, and of crawling movements in larvae of the weevil Rhynchophorus ferrugineus.
Neural Control of Gas Exchange Patterns in Insects: Locust Density-Dependent Phases as a Test Case
Plos One, 2013
The adaptive significance of discontinuous gas exchange cycles (DGC) in insects is contentious. Based on observations of DGC occurrence in insects of typically large brain size and often socially-complex life history, and spontaneous DGC in decapitated insects, the neural hypothesis for the evolution of DGC was recently proposed. It posits that DGC is a nonadaptive consequence of adaptive down-regulation of brain activity at rest, reverting ventilatory control to patterngenerating circuits in the thoracic ganglia. In line with the predictions of this new hypothesis, we expected a higher likelihood of DGC in the gregarious phase of the desert locust (Schistocerca gregaria, Orthoptera), which is characterized by a larger brain size and increased sensory sensitivity compared with the solitary phase. Furthermore, surgical severing of the neural connections between head and thoracic ganglia was expected to increase DGC prevalence in both phases, and to eliminate phase-dependent variation in gas exchange patterns. Using flow-through respirometry, we measured metabolic rates and gas exchange patterns in locusts at 30uC. In contrast to the predictions of the neural hypothesis, we found no phase-dependent differences in DGC expression. Likewise, surgically severing the descending regulation of thoracic ventilatory control did not increase DGC prevalence in either phase. Moreover, connective-cut solitary locusts abandoned DGC altogether, and employed a typical continuous gas exchange pattern despite maintaining metabolic rate levels of controls. These results are not consistent with the predictions of the neural hypothesis for the evolution of DGC in insects, and instead suggest neural plasticity of ventilatory control.