Central Modulatory Neurons Control Fuel Selection in Flight Muscle of Migratory Locust

Abstract

Insect flight is one of the most intense and energy-demanding physiological activities. High carbohydrate oxidation rates are necessary for take-off, but, to spare the limited carbohydrate reserves, long-distance flyers, such as locusts, soon switch to lipid as the main fuel. We demonstrate that before a flight, locust muscles are metabolically poised for take-off by the release of octopamine from central modulatory dorsal unpaired median (DUM) neurons, which increases the levels of the potent glycolytic activator fructose 2,6-bisphosphate in flight muscle. Because DUM neurons innervating the flight muscles are active during rest but selectively inhibited during flight, they stimulate carbohydrate catabolism during take-off but tend to decrease muscle glycolysis during prolonged flight. cAMP-dependent protein kinase A is necessary but not sufficient for signal transduction, suggesting parallel control via a calcium-dependent pathway. Locust flight is the first reported instance of a direct and specific involvement of neuronal activity in the control of muscle glycolysis in working muscle during exercise.

Flight Initiation and Maintenance Deficits in Flies with Genetically Altered Biogenic Amine Levels

“…Previous studies suggested that OA acts as a potent, direct stimulator of flight muscle metabolism (Wegener, 1996;Mentel et al, 2003). Accordingly, we expected that especially prolonged flight would be affected in T␤H mutants, attributable to insufficient fuel supply.…”

“…OA and TA are decarboxylation products of the amino acid tyrosine, with TA as the biological precursor of OA. In insect flight systems, OA assumes a variety of physiological roles affecting central neuron excitability (Ramirez and Pearson, 1991), synaptic transmission (Evans and O'Shea, 1979;Leitch et al, 2003), sensory sensitivity (Matheson, 1997), hormone release (Orchard et al, 1993), and muscle metabolism (Mentel et al, 2003). Almost every organ is equipped with OA receptors (Roeder, 1999).…”

Review of octopamine in insect nervous systems

“…2,4,5 Circulating levels of OCT are increased during "stressful" conditions, such as mobilization of lipids and sugars, so OCT is involved in adjusting an insect's body for a period of extended activity or assisting in recovery from a period of increased energy demand. [8][9][10][11][12][13][14][15] OCT produces a rapid increase in the circulating hemocyte population in response to bacterial challenge in some insects, such as the American cockroach, Periplaneta americana, and the beet armyworm, Spodoptera exigua. 16,17 It is suggested that OCT mediates cellular immune responses such as hemocytic phagocytosis and nodule formation via eicosanoids during bacterial invasion in insects.…”

Variations in the ultrastructure of the flight muscles of the polymorphic cricket, Gryllus firmus (Orthoptera: Gryllidae)

“…In the jargon of the aeronautics industry, flight pushes the envelope of organism design (Dickinson, 1997). Flight muscle is one of the most widely studied flight-related tissues in insects mainly because of the variation in the metabolic activity of the different types of muscle (Sacktor, 1970;Usherwood, 1975, Mentel et al, 2003. All muscles receive excitatory innervation from glutamatergic neurons, inhibitory innervation from GABAergic neurons and modulatory innervation from octopaminergic dorsal unpaired median (DUM) neurons (Biserova & Pfluger, 2004).…”

“…The ultrastructure of the flight muscles, especially those associated with insect growth and development is well described (Herold, 1965;Reedy, 1968;Davies, 1974;Mizisin & Ready, 1986;Novicki, 1989;Reedy & Beall, 1993;Mentel et al, 2003;Biserova & Pfluger, 2004). The juvenile hormone (JH) is critical for both the growth and degeneration of flight muscles (Novicki, 1989;Rose, 2004).…”