Properties of the CNS During the State of Hibernation

Beckman, Alexander L.; Stanton, Toni L.

doi:10.1007/978-94-011-6302-6_2

Cited by 34 publications

(28 citation statements)

References 66 publications

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“…DmpARC neurons of the Siberian hamster are four-to five-fold more active in SD ) and therefore may require replenishment of glutamate for which tanycytes may provide the source of glutamine. Consistent with this idea is the noted presence of glycogen and lipid droplets in tanycytes of other species (Akmayev and Popov, 1977;Lima et al, 2010;Wittkowski and Mueller, 1976) and a seasonal change in the accumulation of glycogen in the hedgehog where glycogen accumulates during hibernation (Wittkowski and Mueller, 1976), a period when neuronal signaling may be greatly diminished (Beckman and Stanton, 1982).…”

Section: Discussionmentioning

confidence: 71%

Photoperiodic regulation of glycogen metabolism, glycolysis, and glutamine synthesis in tanycytes of the Siberian hamster suggests novel roles of tanycytes in hypothalamic function

Nilaweera

Herwig

Bolborea

et al. 2011

Glia

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The objective of this study is to investigate the impact of photoperiod on the temporal and spatial expression of genes involved in glucose metabolism in the brain of the seasonal mammal Phodopus sungorus (Siberian hamster). In situ hybridization was performed on brain sections obtained from male hamsters held in long photoperiod (high body weight and developed testes) or short photoperiod (reduced body weight with testicular regression). This analysis revealed upregulation in expression of genes involved in glycogen and glucose metabolism in short photoperiod and localized to the tanycyte layer of the third ventricle. On the basis of these data and a previously identified photoperiod-dependent increase in activity of neighboring hypothalamic neurons, we hypothesized that the observed expression changes may reflect alteration in either metabolic fuel or precursor neurotransmitter supply to surrounding neurons. Gene expression analysis was performed for genes involved in lactate and glutamate transport. This analysis showed that the gene for the lactate transporter MCT2 and glutamate transporter GLAST was decreased in the tanycyte layer in short photoperiod. Expression of mRNA for glutamine synthetase, the final enzyme in the synthesis of the neuronal neurotransmitter precursor, glutamine, was also decreased in short photoperiod. These data suggest a role for tanycytes in modulating glutamate concentrations and neurotransmitter supply in the hypothalamic environment.

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Section: Discussionmentioning

confidence: 71%

Photoperiodic regulation of glycogen metabolism, glycolysis, and glutamine synthesis in tanycytes of the Siberian hamster suggests novel roles of tanycytes in hypothalamic function

Nilaweera

Herwig

Bolborea

et al. 2011

Glia

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“…A second hypothesis evaluated in the present study is related to the question of whether hippocampal pyramidal cells send signals over pathways that suppress the ARS (4,16). Supporting this hypothesis are data showing that histamine infusion into the hippocampus can extend a bout of hibernation by ϳ50%.…”

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confidence: 59%

Decreasing temperature shifts hippocampal function from memory formation to modulation of hibernation bout duration in Syrian hamsters

Arant

Goo

Gill

et al. 2011

American Journal of Physiology-Regulatory, Integrative and Comp

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. Decreasing temperature shifts hippocampal function from memory formation to modulation of hibernation bout duration in Syrian hamsters. Am J Physiol Regul Integr Comp Physiol 301: R438 -R447, 2011. First published May 11, 2011 doi:10.1152/ajpregu.00016.2011.-Previous studies in hibernating species have characterized two forms of neural plasticity in the hippocampus, long-term potentiation (LTP) and its reversal, depotentiation, but not de novo long-term depression (LTD), which is also associated with memory formation. Studies have also shown that histamine injected into the hippocampus prolonged hibernation bout duration. However, spillover into the ventricles may have affected brain stem regions, not the hippocampus. Here, we tested the hypothesis that decreased brain temperature shifts the major function of the hippocampus in the Syrian hamster (Mesocricetus auratus) from one of memory formation (via LTP, depotentiation, and de novo LTD) to increasing hibernation bout duration. We found reduced evoked responses in hippocampal CA1 pyramidal neurons following lowfrequency stimulation in young (Ͻ30 days old) and adult (Ͼ60 days old) hamsters, indicating that de novo LTD was generated in hippocampal slices from both pups and adults at temperatures Ͼ20°C. However, at temperatures below 20°C, synchronization of neural assemblies (a requirement for LTD generation) was markedly degraded, implying that de novo LTD cannot be generated in hibernating hamsters. Nonetheless, even at temperatures below 16°C, pyramidal neurons could still generate action potentials that may traverse a neural pathway, suppressing the ascending arousal system (ARS). In addition, histamine increased the excitability of these pyramidal cells. Taken together, these findings are consistent with the hypothesis that hippocampal circuits remain operational at low brain temperatures in Syrian hamsters and suppress the ARS to prolong bout duration, even though memory formation is muted at these low temperatures.long-term depression; long-term potentiation; ascending arousal system; histamine AT ALL STAGES OF THE HIBERNATION cycle, thermogenic effectors are appropriately activated by the central nervous system (CNS) to regulate core and brain temperature (13,16). This preservation of homeostatic temperature regulation has far reaching consequences at both cellular and systemic levels. The low temperature of an animal in hibernation results in reduced neural firing rates throughout the CNS (19,20,28,37), which, together with reduction in metabolic rates of all cells, contributes to energy conservation, allowing the animal to survive in winter when food is scarce (9). Despite lower neuronal firing rates as brain temperature decreases, thermoeffector pathways in the CNS (30, 33) continue to control brown fat thermogenesis, shivering, and vasomotor tone, and thus regulate body temperature at all stages of hibernation, including deep hibernation (13, 16). In the present study, we investigated the possibility that regulated brain temperature shifts the ma...

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“…In fact, the hippocampus, among other limbic structures, displays continuous EEG activity throughout the hibernation bout and is one of the first brain structures to regain its normal electrical activity before the arousal process begins (11). These observations contrast with the relative electrical silence in cortical and midbrain areas during hibernation and underscore the subordination of the reappearance of their electrical activity to hippocampal control (3,12). A complex structural connectivity within the hippocampus mediates spatial behaviors such as the storage and retrieval of food stores by birds and mammals within their defined territory (13,14).…”

mentioning

confidence: 93%

“…Hibernating species can adapt to anticipated scarcity in food supply and decreases in ambient temperature by storing food and increasing food intake for several weeks before winter starts (2). Once the animals enter into hibernation, they develop an energy conserving behavior and undergo deep bouts of hypothermia (or torpor) alternated with short euthermic intervals termed periodic arousals (3). By using fat stores as their primary source of energy and reducing carbohydrate metabolism, hibernating mammals sustain vital functions during prolonged periods without feeding and support periodic rewarming during interbout arousals (4).…”

mentioning

confidence: 99%

Rapid and reversible changes in intrahippocampal connectivity during the course of hibernation in European hamsters

Magariños

McEwen

Saboureau

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

124

102

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The hippocampal formation is a highly plastic brain structure that undergoes structural remodeling in response to internal and external challenges such as metabolic imbalance and repeated stress. We investigated whether the extreme alterations in metabolic status that occur during the course of hibernation in European hamsters cause structural changes in the dendritic arborizations of the CA3 pyramidal neurons and their main excitatory afferents, the mossy fiber terminals (MFT), that originate in the dentate gyrus. We report that apical, but not basal, dendritic trees of Golgiimpregnated CA3 principal neurons are significantly shorter, less branched, and less spiny in hypothermic hamsters compared with active animals. After the induction of arousal from torpor, within 2 h, the apical dendritic lengths, branching patterns, and spine density estimations returned to levels found in active, euthermic hamsters. The ultrastructure of MFT in hibernating hamsters showed a significant reduction in synaptic vesicle density and in the percentage of MFT area covered by spine profiles. Awakened hamsters showed restoration of MFT morphology to that seen in active animals. MFT of torpid animals also showed a significant increase in the percentage area of mitochondrial profiles that remained higher 3 h after induced arousal from hibernation compared with euthermic controls. Thus, the torpid/awakening cycle of the hibernating European hamster causes a rapid and reversible morphological reorganization of intrahippocampal subregions involved in information processing. The reported reductions in morphological connectivity between the dentate gyrus and the CA3 subregions could underlie the cessation of exploratory activity and spatial navigation skills during hibernation.CA3 region ͉ hippocampus ͉ mossy fibers ͉ spines ͉ Golgi impregnation H ibernation is a highly regulated physiological response to adverse environmental conditions characterized by hypothermia and drastic reductions of metabolic rate (1). Hibernating species can adapt to anticipated scarcity in food supply and decreases in ambient temperature by storing food and increasing food intake for several weeks before winter starts (2). Once the animals enter into hibernation, they develop an energy conserving behavior and undergo deep bouts of hypothermia (or torpor) alternated with short euthermic intervals termed periodic arousals (3). By using fat stores as their primary source of energy and reducing carbohydrate metabolism, hibernating mammals sustain vital functions during prolonged periods without feeding and support periodic rewarming during interbout arousals (4).The physiological mechanisms triggering hibernation are very complex and far from being well known. Its seasonal occurrence is primarily regulated by the annual photoperiodic variations, and the neuroendocrine and neural mechanisms involved have been partly identified (5-8). The hippocampus, a target brain region for stressful challenges and adrenal steroids (9), has been postulated as a key structure in th...

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Properties of the CNS During the State of Hibernation

Cited by 34 publications

References 66 publications

Photoperiodic regulation of glycogen metabolism, glycolysis, and glutamine synthesis in tanycytes of the Siberian hamster suggests novel roles of tanycytes in hypothalamic function

Photoperiodic regulation of glycogen metabolism, glycolysis, and glutamine synthesis in tanycytes of the Siberian hamster suggests novel roles of tanycytes in hypothalamic function

Decreasing temperature shifts hippocampal function from memory formation to modulation of hibernation bout duration in Syrian hamsters

Rapid and reversible changes in intrahippocampal connectivity during the course of hibernation in European hamsters

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