Suppression of spikes during posttetanic hyperpolarization in auditory neurons: The role of temperature, Ih currents, and the Na+-K+-ATPase pump

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Abstract

In vivo recordings from postsynaptic neurons in the medial nucleus of the trapezoid body (MNTB), an auditory brain stem nucleus, show that acoustic stimulation produces a burst of spikes followed by a period of hyperpolarization and suppressed spiking activity. The underlying mechanism for this hyperpolarization and reduced spiking is unknown. Furthermore, the mechanisms that control excitability and resting membrane potential are not fully determined for these MNTB neurons. In this study we investigated the excitability of principal neurons from the MNTB after high-frequency afferent fiber stimulation, using whole cell recordings from postnatal day 15-17 rat brain stem slices. We found that Na+-K+-ATPase activity mediates a progressive hyperpolarization during a prolonged tetanic train and a posttetanic hyperpolarization (PTH) at the end of the train, when postsynaptic action potentials failed to fire. Raising the temperature to more physiological levels (from 22 to 35°C) depolarized the resting membrane potential of both presynaptic and postsynaptic cells and decreased the latency of action potential firing during PTH. Higher temperatures also reduced the presynaptic calyx action potential failure rates by 50% during presynaptic PTH, thus increasing the safety-factor for presynaptic spiking. The effect of temperature on hyperpolarization-activated cation current (Ih) is reflected in the resting potential at both preand postsynaptic neurons. We thus propose that temperature-sensitive Na+-K+-ATPase activity and Ih contribute to set the resting membrane potential and produce a brief period of suppressed spiking (or action potential failures) after a prolonged high-frequency afferent tetanus.

Original languageEnglish (US)
Pages (from-to)1924-1932
Number of pages9
JournalJournal of Neurophysiology
Volume108
Issue number7
DOIs
Publication statusPublished - Oct 1 2012

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Keywords

  • Calyx of Held synapse
  • Mammalian body temperature
  • Medial nucleus of the trapezoid body principal cells
  • Rat
  • Resting membrane potential

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

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