Intrahippocampal histamine delays arousal from hibernation

Sallmén, Tina; Lozada, Adrian F.; Beckman, Alexander L.; Panula, Pertti

doi:10.1016/s0006-8993(02)04235-x

Cited by 21 publications

(18 citation statements)

References 21 publications

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“…3 and 4) and single cell action potentials (Fig. 5) support Sallmen's proposals (35), as they show that pyramidal cells can generate signals over a large range of temperatures, confirming observations noted in previous studies on pyramidal cell populations in Syrian hamsters (8,21,22). In our slice preparation, afferent fibers from other regions of the CNS are severed, allowing us to conclude that histamine directly excites CA3 pyramidal cells, a finding consistent with Sallmen et al's proposal.…”

Section: R443 Temperature Shifts Hippocampal Function In Syrian Hamsterssupporting

confidence: 81%

“…5) and that histamine directly increased pyramidal cell excitability (Fig. 6), coupled with work showing that histamine injected into the hippocampus of hibernating ground squirrels prolonged bouts of hibernation (35) support the view that the hippocampus plays a role in this prolongation via suppression of the ARS. Taken together, these studies support the assertion that the hamster hippocampus shifts major functional roles from memory formation in the nonhibernating, euthermic state (T brain ϳ37°C) to suppression of the ARS in the hibernating state (T brain ϳ8°C).…”

Section: Discussionsupporting

confidence: 61%

“…Supporting this hypothesis are data showing that histamine infusion into the hippocampus can extend a bout of hibernation by ϳ50%. Although these data are consistent with histamine activation of hippocampal pathways that inhibit the ARS (35), they are also consistent with histamine spilling over into the lateral ventricles and moving downstream to act primarily on brain stem regions adjacent to the third ventricle. Thus, we tested the hypothesis that hippocampal pyramidal neurons can still generate action po-tentials at low temperatures and that histamine increases the excitability of this population of neurons.…”

supporting

confidence: 60%

“…Extending these observations to hibernating species, a few reviews (3,16) include models depicting enhanced hippocampal activity inhibiting the ARS and include the hippocampus as one of many brain regions that continue to operate at reduced levels during hibernation. Further support for these hibernation models linking the hippocampus to the ARS comes from the work of Sallmen et al (35). They found that histamine infusion into the hippocampus extended a bout of hibernation by ϳ50%, suggesting that at low brain temperatures, histamine excited hippocampal pyramidal cells, which, in turn, inhibited the ARS and prolonged bout duration.…”

Section: R443 Temperature Shifts Hippocampal Function In Syrian Hamstersmentioning

confidence: 92%

“…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 major function of the hippocampus from one of memory formation in euthermic hamsters (11,27) to one of extending hibernation bout duration (35). Such a functional shift could provide additional energy savings.…”

mentioning

confidence: 97%

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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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Section: R443 Temperature Shifts Hippocampal Function In Syrian Hamsterssupporting

confidence: 81%

Section: Discussionsupporting

confidence: 61%

supporting

confidence: 60%

Section: R443 Temperature Shifts Hippocampal Function In Syrian Hamstersmentioning

confidence: 92%

mentioning

confidence: 97%

See 3 more Smart Citations

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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Spatial and temporal activation of brain regions in hibernation: c‐fos expression during the hibernation bout in thirteen‐lined ground squirrel

Bratincsák¹,

McMullen²,

Miyake³

et al. 2007

J of Comparative Neurology

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Hibernation results in dramatic changes in body temperature and metabolism; however, the central nervous system remains active during deep torpor. By cloning c-fos cDNA from the 13-lined ground squirrel (Spermophilus tridecemlineatus) and using squirrel c-fos mRNA probe for in situ hybridization histochemistry, we systematically analyzed and identified specific brain regions that were activated during six different phases of the hibernation bout. During entrance into torpor, we detected activation of the ventrolateral subdivision of the medial preoptic area ('thermoregulatory center'), and the reticular thalamic nucleus, which is known to inhibit the somatomotor cortex. During torpor, c-fos expression in the cortex was suppressed while the reticular thalamic nucleus remained uniformly active. Throughout torpor the suprachiasmatic nucleus ('biological clock') showed increasing activity, likely participating in phase-change regulation of the hibernation bout. Interestingly, during torpor very strong c-fos activation was seen in the epithelial cells of the choroid plexus and in tanycytes at the third ventricle, both peaking near the beginning of arousal. In arousal, activity of the suprachiasmatic and reticular thalamic nuclei and choroid epithelial cells diminished, while ependymal cells in the lateral and fourth ventricles showed stronger activity. Increasing body temperature during arousal was driven by the activation of neurons in the medial part of the preoptic area. In interbout awake animals, we demonstrated the activation of hypothalamic neurons located in the arcuate nucleus and the dorsolateral hypothalamus, areas involved in food intake. Our observations indicate that the hibernation bout is closely regulated and orchestrated by specific regions of the central nervous system. J. Comp. Neurol. 505:443-458, 2007. (c) 2007 Wiley-Liss, Inc.

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Syrian hamster neuroplasticity mechanisms fail as temperature declines to 15 °C, but histaminergic neuromodulation persists

et al. 2017

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Previous research suggests that hippocampal neurons in mammalian hibernators shift their major function from memory formation at euthermic brain temperatures (T = ~37 °C) to modulation of hibernation bout duration as T decreases. This role of hippocampal neurons during torpor is based in part on in vivo studies showing that histamine (HA) infused into ground squirrel hippocampi lengthened torpor bouts by ~50%. However, it was unclear if HA acted directly on hippocampal neurons or on downstream brain regions via HA spillover into lateral ventricles. To clarify this, we used hippocampal slices to determine if HA would modulate pyramidal neurons at low levels of synaptic activity (as occurs in torpor). We tested the hypotheses that although LTP (a neuroplasticity mechanism) could not be generated at low temperatures, HA (via H2 receptors) would increase population spike amplitudes (PSAs) of Syrian hamster CA1 pyramidal neurons at low stimulation voltages and low temperatures. PSAs were recorded following Schaffer collateral stimulation from subthreshold levels to a maximum response plateau. We found that tetanus evoked LTP at 35 °C but not 15 °C; and at temperatures from 30 to 15 °C, HA significantly enhanced PSA at near threshold levels in slices from non-hibernating hamsters housed in "summer-like" or "winter-like" conditions and from hibernating hamsters. Cimetidine (H2 antagonist) blocked HA-mediated PSA increases in 8 of 8 slices; pyrilamine (H1 antagonist) had no effect in 7 of 8 slices. These results support our hypotheses and show that HA can directly enhance pyramidal neuron excitability via H2 receptors and thus may prolong torpor bouts.

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Intrahippocampal histamine delays arousal from hibernation

Cited by 21 publications

References 21 publications

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

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

Spatial and temporal activation of brain regions in hibernation: c‐fos expression during the hibernation bout in thirteen‐lined ground squirrel

Syrian hamster neuroplasticity mechanisms fail as temperature declines to 15 °C, but histaminergic neuromodulation persists

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