Premium
Adenosine A 1 receptor activates background potassium channels and modulates information processing in olfactory bulb mitral cells
Author(s) -
Rotermund Natalie,
Winandy Svenja,
Fischer Timo,
Schulz Kristina,
Fregin Torsten,
Alstedt Nadine,
Buchta Melanie,
Bartels Janick,
Carlström Mattias,
Lohr Christian,
Hirnet Daniela
Publication year - 2018
Publication title -
the journal of physiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.802
H-Index - 240
eISSN - 1469-7793
pISSN - 0022-3751
DOI - 10.1113/jp275503
Subject(s) - olfactory bulb , adenosine , neuroscience , adenosine a1 receptor , hyperpolarization (physics) , stimulation , adenosine receptor , sensory system , biology , medicine , chemistry , biophysics , endocrinology , receptor , central nervous system , agonist , organic chemistry , nuclear magnetic resonance spectroscopy
Key points Adenosine is a widespread neuromodulator in the mammalian brain, but whether it affects information processing in sensory system(s) remains largely unknown. Here we show that adenosine A 1 receptors hyperpolarize mitral cells, one class of principal neurons that propagate odour information from the olfactory bulb to higher brain areas, by activation of background K + channels. The adenosine‐modulated background K + channels belong to the family of two‐pore domain K + channels. Adenosine reduces spontaneous activity of mitral cells, whereas action potential firing evoked by synaptic input upon stimulation of sensory neurons is not affected, resulting in a higher ratio of evoked firing (signal) over spontaneous firing (noise) and hence an improved signal‐to‐noise ratio. The study shows for the first time that adenosine influences fine‐tuning of the input–output relationship in sensory systems.Abstract Neuromodulation by adenosine is of critical importance in many brain regions, but the role of adenosine in olfactory information processing has not been studied so far. We investigated the effects of adenosine on mitral cells, which are projection neurons of the olfactory bulb. Significant expression of A 1 and A 2A receptors was found in mitral cells, as demonstrated by in situ hybridization. Application of adenosine in acute olfactory bulb slices hyperpolarized mitral cells in wild‐type but not in adenosine A 1 receptor knockout mice. Adenosine‐induced hyperpolarization was mediated by background K + currents that were reduced by halothane and bupivacaine, which are known to inhibit two‐pore domain K + (K2P) channels. In mitral cells, electrical stimulation of axons of olfactory sensory neurons evoked synaptic currents, which can be considered as input signals, while spontaneous firing independent of sensory input can be considered as noise. Synaptic currents were not affected by adenosine, while adenosine reduced spontaneous firing, leading to an increase in the signal‐to‐noise ratio of mitral cell firing. Our findings demonstrate that A 1 adenosine receptors activate two‐pore domain K + channels, which increases the signal‐to‐noise ratio of the input–output relationship in mitral cells and thereby modulates information processing in the olfactory bulb.