High temperatures alter physiological properties of pyramidal cells and inhibitory interneurons in hippocampus

Jennifer A Kim,Barry W Connors

doi:10.3389/fncel.2012.00027

Abstract

Temperature has multiple effects on neurons, yet little is known about the effects of high temperature on the physiology of mammalian central neurons. Hyperthermia can influence behavior and cause febrile seizures. We studied the effects of acute hyperthermia on the immature hippocampus in vitro by recording from pyramidal neurons and inhibitory oriens-lacunosum moleculare (O-LM) interneurons (identified by green fluorescent protein (GFP) expression in the GIN mouse line). Warming to 41°C caused depolarization, spontaneous action potentials, reduced input resistance and membrane time constant, and increased spontaneous synaptic activity of most pyramidal cells and O-LM interneurons. Pyramidal neurons of area CA3 were more strongly excited by hyperthermia than those of area CA1. About 90% of O-LM interneurons in both CA1 and CA3 increased their firing rates at hyperthermic temperatures; interneurons in CA3 fired faster than those in CA1 on average. Blockade of fast synaptic transmission did not abolish the effect of hyperthermia on neuronal excitability. Our results suggest that hyperthermia increases hippocampal excitability, particularly in seizure-prone area CA3, by altering the intrinsic membrane properties of pyramidal cells and interneurons.

Highlights

Temperature is a tightly regulated variable in the mammalian brain
Hyperthermia-induced increases in spiking differed between regions: about 69% of CA3 pyramidal cells and 21% of CA1 cells fired in response to heat ramps (Figure 1B)
Our results show that hyperthermia increases the intrinsic excitability of both excitatory and inhibitory neurons of the hippocampus

Summary

Introduction

Even small physiologic fluctuations in brain temperature are known to alter neuron physiology and function (Moser et al, 1993; Andersen and Moser, 1995). Few studies have looked at the acute effects of high temperatures on the physiology of central mammalian neurons. Some experimental effects ascribed to high temperature may have been due to changes in metabolic demands and hypoxia, which alters neuronal physiology (Kawasaki et al, 1990; Jensen et al, 1991, 1992; Jiang and Haddad, 1992; Applegate et al, 1996; Jensen and Wang, 1996; Jensen and Baram, 2000; Sanchez and Jensen, 2005)

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Results

Conclusion