A-type potassium currents dominate repolarisation of neonatal rat primary auditory neurones in situ
Section snippets
Cochlear slice preparation
The preparation of thick transverse slices of the neonatal rat cochlea has been described elsewhere (Jagger et al., 2000). This technique employs the intra-cochlear infusion of cooled Pluronic F127 NF (BASF, Parsippany, USA), a block copolymer that solidifies to a gel (25% solution in artificial perilymph – see below) at room temperature. The gel supports the cochlear partition during microtome slicing. Cochlear slices were prepared from 2–6-day-old (P2–P6) Wistar rats. Following
Identification of inactivating A-type currents in neonatal rat SGN in situ
Whole-cell voltage clamp recordings were made from 74 SG neurones in cochlear slices from 2–6-day-old rats (P2–P6). Cells had membrane capacitance of 7.8±0.3 pF, uncompensated series resistance 6.0±0.2 MΩ, and an input resistance of 499.4±33.7 MΩ, measured from short 10-mV hyperpolarising pulses (see Experimental procedures). Zero-current potential (Vz) was −58.5±1.0 mV, measured from steady-state current values plotted in current–voltage (I–V) relationships. In all neurones tested,
IAs are present in neonatal SGN in a slice preparation, but are absent in age-matched dissociated neurones
Our experiments indicate that neonatal rat primary auditory neurones express ion channels that mediate transient, or A-type potassium currents (IA; Connor and Stevens, 1971, Rogawski, 1985). The voltage dependence of inactivation of these currents suggests that at the resting potential, around 30% of the total A-type conductance could be activated. At these potentials the A-type currents contributed around 60% of the total current activated by depolarisation. There was considerable variation in
Acknowledgements
This study was supported by the Marsden Fund (Royal Society of New Zealand), the Health Research Council of New Zealand, the Deafness Research Foundation of New Zealand Inc, and the Maurice and Phyllis Paykel Trust.
References (51)
Hyperpolarization-activated current (Ih) in primary auditory neurons
Hear. Res.
(1997)- et al.
Complementary roles of BDNF and NT-3 in vestibular and auditory development
Neuron
(1995) - et al.
Nerve growth factor maintains potassium conductance after nerve injury in adult cutaneous afferent dorsal root ganglion neurons
Neuroscience
(2000) - et al.
The role of neurotrophic factors in regulating the development of inner ear innervation
Trends Neurosci.
(1997) Development of a fast transient potassium current in chick cochlear ganglion neurons
Hear. Res.
(1999)- et al.
A technique for slicing the rat cochlea around the onset of hearing
J. Neurosci. Methods
(2000) - et al.
Calcium currents in dissociated cochlear neurons from the chick embryo and their modification by neurotrophin-3
Neuroscience
(1997) Action potentials and underlying voltage-dependent currents studied in cultured spiral ganglion neurons of the postnatal gerbil
Hear. Res.
(1997)- et al.
Endogenously generated spontaneous spiking activities recorded from postnatal spiral ganglion neurons in vitro
Dev. Brain Res.
(2000) - et al.
The neurotrophins act synergistically with LIF and members of the TGF-β superfamily to promote the survival of spiral ganglia neurons in vitro
Hear. Res.
(1999)
The A-current: how ubiquitous a feature of excitable cells is it?
Trends Neurosci.
Qualitative and quantitative observations of spiral ganglion development in the rat
Hear. Res.
Muscarinic receptor-mediated calcium signaling in spiral ganglion neurons of the mammalian cochlea
Brain Res.
Cloning and functional expression of a TEA-sensitive A-type potassium channel from rat brain
FEBS Lett.
Transient outward currents in cochlear ganglion neurons of the chick embryo
Neuroscience
Postnatal maturation of spiral ganglion neurons: A horseradish peroxidase study
Hear. Res.
Development of Na+- and K+-currents in the cochlear ganglion of the chick embryo
Neuroscience
Early development and maturation of the spiral ganglion
Acta Otolaryngol.
Three types of depolarisation-activated potassium currents in acutely isolated mouse vestibular neurons
J. Neurophysiol.
Extracellular ATP-induced Ca2+ mobilization of type I spiral ganglion cells from the guinea pig cochlea
Acta Otolaryngol.
Molecular diversity of K+ channels
Ann. N. Y. Acad. Sci.
Voltage clamp studies of a transient outward membrane current in gastropod neural somata
J. Physiol.
Changes in the electrical properties of chick ciliary ganglion neurones during embryonic development
J. Physiol.
Regulation of A-currents by cell–cell interactions and neurotrophic factors in developing chick parasympathetic neurones
J. Physiol.
Development of ganglion cell topography in the postnatal cochlea
J. Comp. Neurol.
Cited by (39)
Time-dependent activity of primary auditory neurons in the presence of neurotrophins and antibiotics
2017, Hearing ResearchCitation Excerpt :Both UT and NT10 neurons shift from a unitary/phasic profile towards a rapidly-adapting/transient profile over time, whilst NT50 neurons begin with both unitary/phasic and rapidly-adapting/transient activity at 1 DIV, that becomes spread across all categories by 3 DIV. This pattern of firing, namely a predominance of the phasic or unitary/rapidly-adapting profile at 1-2 DIV, has been reported previously by us and others in SGNs from early postnatal mouse (Sun and Salvi, 2009) gerbil (Lin, 1997) and rat (Needham et al., 2012; Wright et al., 2016), adult guinea-pig (Chen, 1997; Szabo et al., 2002) and post-hearing mouse (Smith et al., 2015), as well as acutely-isolated rat SGNs in situ (Jagger and Housley, 2002). Our observation that there is an increase in the slowly-adapting, or transient and tonic profiles with time is consistent with a previous report indicating that time-in-culture influences firing rate (Sun and Salvi, 2009).
Combined application of brain-derived neurotrophic factor and neurotrophin-3 and its impact on spiral ganglion neuron firing properties and hyperpolarization-activated currents
2012, Hearing ResearchCitation Excerpt :Therefore, in order to maintain the functional status quo of SGNs in a clinical setting, a combined application of BDNF and NT3 might be preferred. The predominance of the rapidly-adapting neurons across our population of SGNs is also an outcome that is consistent with earlier reports of SGN activity in the rat (Jagger and Housley, 2002), guinea-pig (Chen, 1997; Szabo et al., 2002), gerbil (Lin, 1997) and mouse (Sun and Salvi, 2009), in which SGNs that are acutely isolated, in cochlear slices or cultured for only several days typically exhibit a rapidly-adapting profile. Alternatively, studies using cochlear explants cultured for 5–7 days report a higher proportion of slowly-adapting neurons (Adamson et al., 2002b; Liu and Davis, 2007; Mo and Davis, 1997a, 2002).
Complex primary afferents: What the distribution of electrophysiologically-relevant phenotypes within the spiral ganglion tells us about peripheral neural coding
2011, Hearing ResearchCitation Excerpt :This evolution in our view of sensory processing has occurred for the auditory system as well. Before we and others began the examination of spiral ganglion neurons with intracellular recordings in order to characterize their intrinsic electrophysiological features (Chen, 1997; Chen and Davis, 2006; Davis, 1996; Garcia-Diaz, 1999; Hisashi et al., 1995; Jagger and Housley, 2002; Jimenez et al., 1997; Lin, 1997; Lin and Chen, 2000; Mo et al., 2002; Mo and Davis, 1997a; Moore et al., 1996; Santos-Sacchi, 1993; Sheppard et al., 1992; Szabo et al., 2002; Yamaguchi and Ohmori, 1990), the general view of the field was that all type I neurons that composed the ganglion were identical. This was based upon the wealth of in vivo recordings revealing that neurons fire in a similar fashion to pure tone stimuli (Kiang et al., 1965, 1984; Sachs et al., 1974).
K<inf>v</inf>7-type channel currents in spiral ganglion neurons: Involvement in sensorineural hearing loss
2010, Journal of Biological ChemistryCitation Excerpt :Several plausible mechanisms can be conceived to explain mutations at multiple sites in Kv7.4 channels that result in SGN degeneration associated with DFNA2 (9). One model will assert that because the expression pattern of several K+ channels, such as Kv4.2, Kv1.1, Kv3.1, and Ca2+-dependent K+ channels in SGNs, show distinct apico-basal gradient (34–37), and in DFNA2 the brunt of reduced activity of Kv7.4 is manifested first in basal neurons. Consequently, increased membrane depolarization ensues, followed by sustained Ca2+ influx through voltage-gated Ca2+ channels resulting in Ca2+-induced cell death.
Voltage-gated K<sup>+</sup> channel (Kv) subunit expression of the guinea pig spiral ganglion cells studied in a newly developed cochlear free-floating preparation
2008, Brain ResearchCitation Excerpt :Other studies also noticed the presence of this current component (i.e. Sheppard et al., 1992), and it has also been described that the expression of a transient current showed significant age dependence: it appeared on the 10th day of the embryonic development, then its amplitude increased afterwards (Garcia-Díaz, 1999). Moreover, the availability and function of the transient K+ current expressed by rat SGCs were clearly demonstrated in a cochlear slice preparation (Jagger and Housley, 2002). The amplitude of the transient current was substantial: approximately 60% of the total current produced from near the resting membrane potential was generated by the relevant channels.