Thermal stress and neural function: adaptive mechanisms in insect model systems

Robertson, R. Meldrum

doi:10.1016/j.jtherbio.2004.08.073

Cited by 81 publications

(79 citation statements)

References 55 publications

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“…The effects of extreme high temperature on neural processes can be divided into two main types: those that have immediate consequences as a result of the Q 10 relationships of the rates of neural phenomena such as the opening and closing of ion channels; and those that have a temporal component reflecting an accumulating disturbance such as gradual protein denaturation or the loss of ionic equilibria (Robertson, 2004). The increase in swim cycle frequency with increasing temperature is not surprising, because this is a well established property of CPGs (Walker, 1975;Tryba and Ramirez, 2003) that is due to the reduction of conduction and synaptic delays between elements in the circuit (Robertson, 2004).…”

Section: Discussionmentioning

confidence: 99%

“…The increase in swim cycle frequency with increasing temperature is not surprising, because this is a well established property of CPGs (Walker, 1975;Tryba and Ramirez, 2003) that is due to the reduction of conduction and synaptic delays between elements in the circuit (Robertson, 2004). The profound decrease in swim episode duration with increasing temperature is not as easy to explain.…”

Section: Discussionmentioning

confidence: 99%

“…Many different processes are likely to be implicated, including the failure to generate action potentials, the increased likelihood of conduction failure at axonal regions of low safety factor, and the failure of synaptic transmission (Janssen, 1992;Robertson, 2004). An important common feature of all of these possibilities is a dysregulation of ion homeostasis or conductance.…”

Section: Discussionmentioning

confidence: 99%

“…Protective mechanisms targeting vital motor activities such as ventilation, predator evasion, and locomotion out of regions of high temperature are clearly selectively advantageous (Robertson, 2004). Long-term processes of acclimation (Johnston and Temple, 2002) can modify neuronal properties and change optimal temperature ranges (Behan-Martin et al, 1993).…”

Section: Introductionmentioning

confidence: 99%

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The Nitric Oxide/cGMP Pathway Tunes the Thermosensitivity of Swimming Motor Patterns inXenopus laevisTadpoles

Robertson

Sillar²

2009

J. Neurosci.

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We investigated the role of the nitric oxide (NO)/cGMP pathway in setting thresholds for failure and recovery during hyperthermic stress of the swimming central pattern generator of immobilized Xenopus tadpoles (stage 42). We recorded swimming motor patterns induced by tail skin stimulation (TS) (1 ms current pulse) or by bath application of 50 M NMDA. Swimming rhythm frequency increased in a linear manner with increasing temperature. In the presence of the NO donor S-nitroso-N-acetylpenicillamine (SNAP), recovery from hyperthermic failure was greatly slowed, often taking longer than the duration of the experiment. Pharmacological activation of the NO/cGMP pathway using SNAP or 8-bromo-cGMP (1) decreased the duration of TS-evoked swim episodes; (2) decreased the temperature threshold for hyperthermic circuit failure; (3) decreased the temperature at which the circuit recovered; and (4) increased the time taken to recover. Pharmacological inhibition of the NO/cGMP pathway using the NO scavenger CPTIO, the nitric oxide synthase (NOS) inhibitor L-NAME or the guanylyl cyclase inhibitor ODQ (1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one) had the opposite effects. NMDA rhythms were more resistant to hyperthermic failure than TS-evoked swim episodes, but the effects of SNAP on the temperature sensitivity of swimming evoked by NMDA were similar to those on TS-evoked swimming, suggesting that drug effects occur on central patterngenerating networks rather than sensory pathways. We conclude that the NO/cGMP pathway is involved in setting the threshold temperatures for hyperthermic failure and subsequent recovery of fictive swimming in tadpoles, and we suggest that this is part of a variable response to prevent overexcitation during abiotic stress under different environmental conditions.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Nitric Oxide/cGMP Pathway Tunes the Thermosensitivity of Swimming Motor Patterns inXenopus laevisTadpoles

Robertson

Sillar²

2009

J. Neurosci.

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“…Thermotolerance of the circuit can be improved by stress preconditioning using heat shock, anoxia, or cold shock and is mimicked by bath application of serotonin (Newman et al, 2003). At the moment of heatinduced rhythm failure, there is an abrupt rise in extracellular potassium [K ϩ ] o in the MTG from ϳ11 to Ͼ40 mM; recovery of the rhythm is reliably associated with time-dependent restoration of the [K ϩ ] o gradient with HS locusts showing more rapid recovery (Robertson, 2004). The mechanisms that coordinate such HS-mediated thermotolerance are unknown, and a possibility we examine here is that amines such as octopamine (OA) are involved.…”

Section: Introductionmentioning

confidence: 99%

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

Armstrong

Shoemaker²,

Money³

et al. 2006

J. Neurosci.

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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 Ϫ4 M OA) or by injections into the hemocoel (2 g/10 l 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 (Oct␤R 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 synthesisdependent physiological adaptations to protect CNS function during heat stress by activating a cAMP/PKA pathway.

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Targeting HSP70 to motoneurons protects locomotor activity from hyperthermia in Drosophila

Xiao

Mileva‐Seitz

Seroude

et al. 2007

Developmental Neurobiology

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Heat shock preconditioning can enhance locomotor and synaptic performance during subsequent hyperthermia. The molecular basis underlying this neural phenotypic modification is largely unknown. Here we report that directing the expression of the 70 kDa heat shock protein (HSP70) to motoneurons protected larval locomotor activity of Drosophila. Tissue-specific expression showed that motoneurons were critical for developing HSP70-mediated thermoprotection of locomotor activity, whereas peripheral sensory neurons, dopaminergic neurons, serotonergic neurons, and muscle cells alone were insufficient. Targeting HSP70 to motoneurons caused structural plasticity of axonal terminals associated with increased transmitter release at neuromuscular junctions at high temperature. The thermoprotection induced by motoneuronal expression of HSP70 mimicked the protective effect of a prior heat shock (36 degrees C, 1 h; 25 degrees C, 1 h) but the effects of heat shock and motoneuronal expression of HSP70 were not additive. In the absence of heat shock pretreatment, ubiquitously expressed transgenic HSP70 activated the transcription of endogenous hsp70 genes. These results demonstrate that motoneurons were critical for HSP70-mediated thermoprotection, and that transgenic HSP70 activated the transcription of endogenous hsp70 in motoneurons with the result that a mix of transgenic and endogenous HSP70 conferred thermoprotection in Drosophila larva.

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Thermal stress and neural function: adaptive mechanisms in insect model systems

Cited by 81 publications

References 55 publications

The Nitric Oxide/cGMP Pathway Tunes the Thermosensitivity of Swimming Motor Patterns inXenopus laevisTadpoles

The Nitric Oxide/cGMP Pathway Tunes the Thermosensitivity of Swimming Motor Patterns inXenopus laevisTadpoles

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

Targeting HSP70 to motoneurons protects locomotor activity from hyperthermia in Drosophila

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