Octopamine stabilizes conduction reliability of an unmyelinated axon during hypoxic stress

Abstract

Mechanisms that could mitigate the effects of hypoxia on neuronal signaling are incompletely understood. We show that axonal performance of a locust visual interneuron varied depending on oxygen availability. To induce hypoxia, tracheae supplying the thoracic nervous system were surgically lesioned and action potentials in the axon of the descending contralateral movement detector (DCMD) neuron passing through this region were monitored extracellularly. The conduction velocity and fidelity of action potentials decreased throughout a 45-min experiment in hypoxic preparations, whereas conduction reliability remained constant when the tracheae were left intact. The reduction in conduction velocity was exacerbated for action potentials firing at high instantaneous frequencies. Bath application of octopamine mitigated the loss of conduction velocity and fidelity. Action potential conduction was more vulnerable in portions of the axon passing through the mesothoracic ganglion than in the connectives between ganglia, indicating that hypoxic modulation of the extracellular environment of the neuropil has an important role to play. In intact locusts, octopamine and its antagonist, epinastine, had effects on the entry to, and recovery from, anoxic coma consistent with octopamine increasing overall neural performance during hypoxia. These effects could have functional relevance for the animal during periods of environmental or activity-induced hypoxia.

Reduced blood oxygen levels induce changes in low-threshold motor unit firing that align with the individual’s tolerance to hypoxia

“…Although the direct consequences of hypoxia on spinal motoneurons have not been studied, in vitro examination of orexin neurons from the lateral hypothalamus (Dergacheva et al 2016), the descending contralateral movement detector neuron of the thorax (Money et al 2016), and hippocampal CA1 neurons (Gu and Haddad 2001) confirms that hypoxia also causes reductions in neuronal excitability. This is evident from hyperpolarization, rapid depression of firing rates, and differences in passive properties of the neuron such as changes in resting membrane potential and Na ϩ channel expression (Dergacheva et al 2016;Gu and Haddad 2001;Money et al 2016). However, it must be noted that isolated neuron preparations do not reflect the multitude of factors that can regulate the output of motoneurons.…”

Two extended haplotype blocks are associated with adaptation to high altitude habitats in East African honey bees

“…In particular, octopamine plays a major role in olfactory learning and memory formation in the honey bee [ 50 ], important tasks for adapting to different environmental conditions. Interestingly, octopamine has also been shown to be important for stabilizing signaling integrity during hypoxic and thermal stress in other insects [ 82 , 83 ]. The four octopamine receptor genes located within r7 have many fixed differences between highland and lowland bees.…”

Disentangling Ethiopian Honey Bee (Apis mellifera) Populations Based on Standard Morphometric and Genetic Analyses

“…By conducting a whole-genome analysis on mountain forest (A. m. monticola) and savannah (A. m. scutellata) honey bees of Kenya, Wallberg et al (2017) [6] identified an intriguing genomic region (denoted as r7) within the gene octopamine receptor beta-2R (LOC412896) located near a potential chromosomal breakpoint, showing striking variability between A. m. monticola and A. m. scutellata. Octopamine stabilizes hypoxia [24] and hypothermia [25] in locusts. In honey bees, it modulates responses to sucrose [26] and learning odors [27], visuals [28] and nursing [29] behaviors and the thermoregulatory fanning response [30].…”