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The Journal of Neuroscience, November 22, 2006, 26(47):12118-12126; doi:10.1523/JNEUROSCI.3347-06.2006

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Behavioral/Systems/Cognitive
Octopamine Mediates Thermal Preconditioning of the Locust Ventilatory Central Pattern Generator via a cAMP/Protein Kinase A Signaling Pathway

Gary A. B. Armstrong, Kelly L. Shoemaker, Tomas G. A. Money, and R. Meldrum Robertson

Department of Biology, Queen's University, Kingston, Ontario, Canada K7L 3N6

Correspondence should be addressed to Gary A. B. Armstrong at the above address. Email: armstrog{at}biology.queensu.ca

We investigated the role of biogenic amines in generating thermoprotection of the ventilatory motor pattern circuitry in Locusta migratoria. Levels of octopamine (OA) and dopamine (DA) in the metathoracic ganglion decreased during heat stress. We measured the thermosensitivity of central pattern generation in response to a ramped increase of temperature in semi-intact preparations. OA, DA, and tyramine (TA) were either bath applied or injected into the locust hemocoel 4–8 h before testing. Neither TA nor DA modified the thermotolerance of ventilatory motor pattern generation. However, OA treatment by bath applications (10^–4 M OA) or by injections into the hemocoel (2 µg/10 µl OA) mimicked heat shock preconditioning and improved the thermotolerance of the motor pattern by increasing the failure temperature and by decreasing the time taken to recover operation after a return to room temperature. Heat shock-induced thermoprotection was eradicated in locusts preinjected with epinastine (OctR antagonist). Neuropil injections of the cAMP agonist and protein kinase A (PKA) activator, Sp-cAMPs, both conferred thermoprotection in control locusts and rescued thermoprotection in epinastine-treated HS locusts. Similar injections of the PKA inhibitor Rp-cAMPs blocked the thermoprotective effect of bath-applied OA. Octopamine-mediated thermoprotection was also abolished with neuropil injections of cycloheximide or actinomycin D, indicating a requirement for transcription and translation. We conclude that OA has a crucial role in triggering protein synthesis-dependent physiological adaptations to protect CNS function during heat stress by activating a cAMP/PKA pathway.

Key words: insect; heat shock; temperature; thermotolerance; motor pattern; biogenic amine; cAMP; PKA

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Received Aug. 3, 2006; revised Sept. 15, 2006; accepted Oct. 8, 2006.

Correspondence should be addressed to Gary A. B. Armstrong at the above address. Email: armstrog{at}biology.queensu.ca

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