Secondary Metabolites and Amino Acids in the Neocortex of the Long-Tailed Ground Squirrel Urocitellus undulatus at Different Stages of Hibernation

Abstract

This study continues our previous research aimed at investigating changes in the pools of amino acids in the myocardium of the ground squirrel during winter torpor. Neurochemical profiles of amino acids and the secondary metabolites (taurine, phosphoserine, and cysteic acid) were explored in the neocortex of the ground squirrel at different stages of torpor: in the beginning of torpor (2–3 days) and during prolonged torpor (9–10 days), as well as during short-term winter arousal (winter activity, euthermia). Reduced excitatory neurotransmitter levels (glutamate by 7% and 14%; aspartate by 25% and 52% in a coordinated manner and the increased level of GABA, the main transmission inhibitor (by 50% and 67%) were observed from the onset of the torpor entry and at the end of the torpor arousal, respectively. Alanine, which was formed in negligible amounts in the neocortex in the summer season, increased at the initial stage of hibernation and after multiday torpor bout (by 98% and 126%, respectively), indicating a partial switch to anaerobic glycolysis. Short-term interbout euthermia returned levels of these substances back to normal. The behavior of glutamate and aspartate, the anaplerotic substrates, that supported cycling of the tricarboxylic acid cycle during torpor and winter activity periods was like their responses in the myocardium, though differed quantitatively. The responses of the neuromodulators such as glycine, threonine, and lysine differed radically when compared to their responses in the myocardium. No changes in taurine and phosphoserine pools were detected, but the level of cysteic acid decreased compared to the summer control from 0.51 ± 0.06 μmol/g to 0.07 ± 0.01 μmol/g at the end of torpor, while during winter euthermia it became 2 times lower than the summer level. Our data suggest that metabolic pathways involving anaplerotic amino acids of the neocortex are more active than the myocardium during winter torpor, while the pools of neuromodulators that regulate inhibition processes, increase.