The Influence of Cold Temperature on Cellular Excitability of Hippocampal Networks

Elvira de la Peña, Annika Mälkiä, Hugo Vara, Rebeca Caires Mugarra, Juan J. Ballesta, Carlos Belmonte, Felix Viana

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

The hippocampus plays an important role in short term memory, learning and spatial navigation. A characteristic feature of the hippocampal region is its expression of different electrical population rhythms and activities during different brain states. Physiological fluctuations in brain temperature affect the activity patterns in hippocampus, but the underlying cellular mechanisms are poorly understood. In this work, we investigated the thermal modulation of hippocampal activity at the cellular network level. Primary cell cultures of mouse E17 hippocampus displayed robust network activation upon light cooling of the extracellular solution from baseline physiological temperatures. The activity generated was dependent on action potential firing and excitatory glutamatergic synaptic transmission. Involvement of thermosensitive channels from the transient receptor potential (TRP) family in network activation by temperature changes was ruled out, whereas pharmacological and immunochemical experiments strongly pointed towards the involvement of temperature-sensitive two-pore-domain potassium channels (K2P), TREK/TRAAK family. In hippocampal slices we could show an increase in evoked and spontaneous synaptic activity produced by mild cooling in the physiological range that was prevented by chloroform, a K2P channel opener. We propose that cold-induced closure of background TREK/TRAAK family channels increases the excitability of some hippocampal neurons, acting as a temperature-sensitive gate of network activation. Our findings in the hippocampus open the possibility that small temperature variations in the brain in vivo, associated with metabolism or blood flow oscillations, act as a switch mechanism of neuronal activity and determination of firing patterns through regulation of thermosensitive background potassium channel activity.

Original languageEnglish (US)
Article numbere52475
JournalPloS one
Volume7
Issue number12
DOIs
StatePublished - Dec 31 2012

Fingerprint

hippocampus
Temperature
Hippocampus
Brain
temperature
Chemical activation
potassium channels
brain
Tandem Pore Domain Potassium Channels
cooling
Cooling
Transient Receptor Potential Channels
synaptic transmission
Primary Cell Culture
Potassium Channels
action potentials
Chloroform
Short-Term Memory
Cell culture
Metabolism

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • General

Cite this

de la Peña, E., Mälkiä, A., Vara, H., Caires Mugarra, R., Ballesta, J. J., Belmonte, C., & Viana, F. (2012). The Influence of Cold Temperature on Cellular Excitability of Hippocampal Networks. PloS one, 7(12), [e52475]. https://doi.org/10.1371/journal.pone.0052475

The Influence of Cold Temperature on Cellular Excitability of Hippocampal Networks. / de la Peña, Elvira; Mälkiä, Annika; Vara, Hugo; Caires Mugarra, Rebeca; Ballesta, Juan J.; Belmonte, Carlos; Viana, Felix.

In: PloS one, Vol. 7, No. 12, e52475, 31.12.2012.

Research output: Contribution to journalArticle

de la Peña, E, Mälkiä, A, Vara, H, Caires Mugarra, R, Ballesta, JJ, Belmonte, C & Viana, F 2012, 'The Influence of Cold Temperature on Cellular Excitability of Hippocampal Networks', PloS one, vol. 7, no. 12, e52475. https://doi.org/10.1371/journal.pone.0052475
de la Peña, Elvira ; Mälkiä, Annika ; Vara, Hugo ; Caires Mugarra, Rebeca ; Ballesta, Juan J. ; Belmonte, Carlos ; Viana, Felix. / The Influence of Cold Temperature on Cellular Excitability of Hippocampal Networks. In: PloS one. 2012 ; Vol. 7, No. 12.
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