Cochlear nucleusIn the ventral cochlear nucleus Kv1.1 and subunits of HCN1 are colocalized at surfaces of neurons that have low-voltage-activated and hyperpolarization-activated conductances
Section snippets
Mice
Mice of the outbred ICR strain and obtained from Sprague–Dawley (Madison, WI, USA) were used in these studies. All animal protocols were approved by the Institutional Animal Care and Use Committee of the School of Medicine and Public Health at the University of Wisconsin, Madison and conform with the guidelines established by the National Institutes of Health in the USA, Care and Use of Laboratory Animals (NIH publications No. 80-23. Care was taken to use as few mice as possible and to cause
Electrophysiology
Whole-cell patch-clamp recordings in the voltage-clamp mode reveal the properties of the ion channels that mediate IKL and Ih. Examples of such recordings are illustrated in Fig. 1. In all recordings some currents were blocked pharmacologically: 0.25 mM Cd2+ blocked voltage-gated Ca2+ currents, 1 μM TTX blocked voltage-gated Na+ currents, 40 μM DNQX blocked spontaneous EPSCs through AMPA receptors, and 1 μM strychnine blocked spontaneous IPSCs through glycine receptors. The upper panels
Discussion
There was a strong correlation between electrophysiological measurements of voltage-sensitive conductances and surface labeling for subunits of ion channels that mediate those conductances. The octopus cells that have exceptionally strong gKL and gh have surfaces that are the most brightly labeled for HCN1 that is colocalized with Kv1.1 at the surfaces of cell bodies and dendrites. An unexpected finding was that cells whose labeling for these antigens resembles that of octopus cells were found
Conclusion
In summary, the present study leads to the following conclusions. 1) Surface labeling for Kv1.1 and HCN1 is correlated with the magnitude of maximal gKL and gh measured in neurons in those areas. Surface labeling is strong for octopus cells, and for a population of cells that is sparsely distributed over the VCN that might correspond to D stellate cells, less strong for bushy cells, and least for T stellate cells. 2) In octopus cells, and probably also bushy cells, gKL and gh are likely to be
Acknowledgments
We are most grateful to Ed Chapman for giving us the opportunity to use the confocal microscope and to Camin Dean and Felix Yeh who answered our questions patiently and graciously. Two anonymous reviewers pointed out several significant shortcomings and omissions in a very nice way; thank you! We thank Samantha Wright for her valuable comments. We also thank Ravi Kochhar and the departmental office staff for their continuing support. This work was supported by a grant from NIH DC 00176.
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Cited by (44)
2.35 - Coding of Temporal Information
2020, The Senses: A Comprehensive Reference: Volume 1-7, Second EditionModulatory influences on time-coding neurons in the ventral cochlear nucleus
2019, Hearing ResearchThe ion channels and synapses responsible for the physiological diversity of mammalian lower brainstem auditory neurons
2019, Hearing ResearchCitation Excerpt :The low membrane resistance creates a fast membrane time constant that favors the speed and precision of firing, and impairs the integration of synaptic potentials, resulting in a single post-synaptic action potential per presynaptic action potential (Oertel, 1983; Smith and Rhode, 1987). The presence of a prominent hyperpolarization activated cationic current (Ih) produced by the expression of the subunits HCN1 and HCN4 is the main contributor for the low membrane resistance of bushy cells (Schwarz and Puil, 1997; Leao et al., 2006; Cao et al., 2007; Oertel et al., 2008). Additionally, a reduced expression of voltage-dependent sodium conductances in the soma of bushy cells enhances precision and fidelity of action potential firing in these neurons (Yang et al., 2016).
Cellular Computations Underlying Detection of Gaps in Sounds and Lateralizing Sound Sources
2017, Trends in NeurosciencesGenetic perturbations suggest a role of the resting potential in regulating the expression of the ion channels of the KCNA and HCN families in octopus cells of the ventral cochlear nucleus
2017, Hearing ResearchCitation Excerpt :The HCN channels that mediate Ih are permeable to both Na+ and K+ and have a reversal potential of −40 mV so that Ih is inward at the resting potential in octopus and many other types of neurons (Banks et al., 1993; Bal and Oertel, 2000). HCN1 and Kv1.1 are colocalized in the somatic and dendritic octopus cell membrane (Oertel et al., 2008; Rusznak et al., 2008; Robbins and Tempel, 2012). In an earlier study we examined mice in which HCN1 was eliminated to alter gh (Cao and Oertel, 2011).
A mechanistic understanding of the role of feedforward inhibition in the mammalian sound localization circuitry
2013, NeuronCitation Excerpt :Thus, the interplay between inhibition and Kv1 channels provides a mechanism that helps preserve the timing of EPSPs while simultaneously sharpening binaural coincidence detection. Kv1-containing K+ channels are broadly expressed in many areas of the brain (Sheng et al., 1994; Wang et al., 1994; Trimmer and Rhodes, 2004) and are found in especially high density in auditory brainstem neurons concerned with the precise coding of temporal information, including the MSO (e.g., Bal and Oertel, 2001; Dodson et al., 2002; Rothman and Manis, 2003; Oertel et al., 2008; Johnston et al., 2010). Mouse knockouts of Kv1.1 show deficits in sound localization (Allen and Ison, 2012), probably reflecting altered excitability and precision in neurons of the superior olivary nuclei and their associated inputs (Brew et al., 2003; Kopp-Scheinpflug et al., 2003; Gittelman and Tempel, 2006).