With oxygen deprivation, the mammalian brain undergoes hyper-activity and neuronal death while this does not occur in the anoxia tolerant goldfish (Carassius auratus). Anoxic survival of the goldfish may rely on neuromodulatory mechanisms to suppress neuronal hyper-excitability. Since γ-aminobutyric acid (GABA) is the major inhibitory neurotransmitter in brain, we decided to investigate its potential role in suppressing the electrical activity of goldfish telencephalic neurons. Utilizing whole-cell patch-clamp recording we recorded the electrical activities of both excitatory (pyramidal) and inhibitory (stellate) neurons. With anoxia, membrane potential (Vm) depolarized in both cell types from −72.2mV to −57.7mV and from −64.5mV to −46.8mV in pyramidal and stellate neurons, respectively. While pyramidal cells remained mostly quiescent, action potential frequency (APf) of the stellate neurons increased 68 fold. Furthermore, the GABAA receptor reversal potential (EGABA) was determined using the gramicidin perforated-patch clamp method and found to be depolarizing in pyramidal (−53.8mV) and stellate neurons (−42.1mV). Although GABA was depolarizing, pyramidal neurons remained quiescent since EGABA is below the action potential threshold (−36mV pyramidal and −38mV stellate neurons). Inhibition of GABAA receptors with gabazine reversed the anoxia mediated response. While GABAB receptor inhibition alone did not affect the anoxic response, co-antagonism of GABAA and GABAB receptors (gabazine and CGP-55848) lead to generation of seizure-like activities in both neuron types. We conclude that with anoxia Vm depolarizes towards EGABA which increases APf in stellate neurons and decreases APf in pyramidal neurons, and that GABA plays an important role in the anoxia-tolerance of goldfish brain.
Stellate and pyramidal neurons in goldfish telencephalon respond differently to anoxia and GABA receptor inhibition
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Nariman Hossein-Javaheri, Michael P. Wilkie, Wudu E. Lado, Leslie T. Buck; Stellate and pyramidal neurons in goldfish telencephalon respond differently to anoxia and GABA receptor inhibition. J Exp Biol 2016; jeb.146605. doi: https://doi.org/10.1242/jeb.146605
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