Abstract
Neuro-anatomical studies in the mammalian cochlea have previously identified a subpopulation of approximately 5 % of primary auditory neurones, designated type II spiral ganglion neurones (sgnII). These neurones project to outer hair cells and their supporting cells, within the 'cochlear amplifier' region. Physiological characterization of sgnII has proven elusive. Whole-cell patch clamp of spiral ganglion neurones in P7-P10 rat cochlear slices provided functional characterization of sgnII, identified by biocytin or Lucifer yellow labelling of their peripheral neurite projections (outer spiral fibres) subsequent to electrophysiological characterisation. SgnII terminal fields comprised multiple outer hair cells and supporting cells, located up to 370 mum basal to their soma. SgnII firing properties were defined by rapidly inactivating A-type-like potassium currents that suppress burst firing of action potentials. Type I spiral ganglion neurones (sgnI), had shorter radial projections to single inner hair cells and exhibited larger potassium currents with faster activation and slower inactivation kinetics, compatible with the high temporal firing fidelity seen in auditory nerve coding. Based on these findings, sgnII may be identified in future by the A-type current. Glutamate-gated somatic currents in sgnII were more potentiated by cyclothiazide than those in sgnI, suggesting differential AMPA receptor expression. ATP-activated desensitising inward currents were comparable in sgn II and sgnI. These data support a role for sgnII in providing integrated afferent feedback from the cochlear amplifier.
MeSH Terms
Animals
Animals, Newborn/physiology
Cell Membrane/physiology
Cochlea/cytology,innervation,physiology
Electrophysiology
In Vitro Techniques
Isoquinolines
Kinetics
Lysine/analogs & derivatives
Membrane Potentials/physiology
Neurons/physiology
Patch-Clamp Techniques
Phenotype
Rats
Spiral Ganglion/cytology,physiology
Chemicals
Isoquinolines
lucifer yellow
biocytin
Lysine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Jagger Daniel J
Department of Physiology, University of Auckland, Private Bag 92019, Auckland, New Zealand.
Housley Gary D
References (28)
28 references, click to expand
-
Organization of AMPA receptor subunits at a glutamate synapse: a quantitative immunogold analysis of hair cell synapses in the rat organ of Corti.
J Neurosci. 1996 Jul 15;16(14):4457-67
PMID: 8699256
-
Expression of AMPA, kainate, and NMDA receptor subunits in cochlear and vestibular ganglia.
J Neurosci. 1995 Mar;15(3 Pt 2):2338-53
PMID: 7891171
-
Action potentials and underlying voltage-dependent currents studied in cultured spiral ganglion neurons of the postnatal gerbil.
Hear Res. 1997 Jun;108(1-2):157-79
PMID: 9213129
-
Peripherin-like immunoreactivity in type II spiral ganglion cell body and projections.
Brain Res. 1998 Sep 14;805(1-2):181-90
PMID: 9733963
-
Synaptic mechanisms for coding timing in auditory neurons.
Annu Rev Physiol. 1999;61:477-96
PMID: 10099698
-
AMPA-preferring glutamate receptors in cochlear physiology of adult guinea-pig.
J Physiol. 1999 Aug 1;518 ( Pt 3):667-80
PMID: 10420005
-
Expression of the P2X(2) receptor subunit of the ATP-gated ion channel in the cochlea: implications for sound transduction and auditory neurotransmission.
J Neurosci. 1999 Oct 1;19(19):8377-88
PMID: 10493739
-
The continuing search for outer hair cell afferents in the guinea pig spiral ganglion.
Hear Res. 1999 Oct;136(1-2):151-8
PMID: 10511634
-
A technique for slicing the rat cochlea around the onset of hearing.
J Neurosci Methods. 2000 Dec 15;104(1):77-86
PMID: 11163413
-
Innervation of supporting cells in the apical turns of the guinea pig cochlea is from type II afferent fibers.
J Comp Neurol. 2001 Jan 8;429(2):289-98
PMID: 11116221
-
A-type potassium currents dominate repolarisation of neonatal rat primary auditory neurones in situ.
Neuroscience. 2002;109(1):169-82
PMID: 11784708
-
Transmitter release at the hair cell ribbon synapse.
Nat Neurosci. 2002 Feb;5(2):147-54
PMID: 11802170
-
ATP-gated currents in rat primary auditory neurones in situ arise from a heteromultimetric P2X receptor subunit assembly.
Neuropharmacology. 2002 Mar;42(3):386-95
PMID: 11897117
-
Firing features and potassium channel content of murine spiral ganglion neurons vary with cochlear location.
J Comp Neurol. 2002 Jun 10;447(4):331-50
PMID: 11992520
-
Horseradish peroxidase injection of physiologically characterized afferent and efferent neurones in the guinea pig spiral ganglion.
Hear Res. 1984 Aug;15(2):113-21
PMID: 6490538
-
Qualitative and quantitative observations of spiral ganglion development in the rat.
Hear Res. 1985 May;18(2):111-20
PMID: 4044415
-
Kainic acid selectively alters auditory dendrites connected with cochlear inner hair cells.
Hear Res. 1985 May;18(2):145-51
PMID: 2864329
-
Hair cell innervation by spiral ganglion neurons in the mouse.
J Comp Neurol. 1987 Jan 22;255(4):560-70
PMID: 3819031
-
Morphology of labeled afferent fibers in the guinea pig cochlea.
J Comp Neurol. 1987 Jun 22;260(4):591-604
PMID: 3611412
-
Central trajectories of type II spiral ganglion neurons.
J Comp Neurol. 1988 Dec 22;278(4):581-90
PMID: 3230171
-
Developmental segregation in the afferent projections to mammalian auditory hair cells.
Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6324-7
PMID: 1631126
-
Hippocampal neurons exhibit cyclothiazide-sensitive rapidly desensitizing responses to kainate.
J Neurosci. 1993 Aug;13(8):3496-509
PMID: 7688040
-
Development of hearing in neonatal rats: air and bone conducted ABR thresholds.
Hear Res. 1993 Sep;69(1-2):236-42
PMID: 8226345
-
Ontogenesis of type II spiral ganglion neurons during development: peripherin immunohistochemistry.
Int J Dev Neurosci. 1993 Aug;11(4):507-12
PMID: 8237466
-
Antidromic responses of single units from the spiral ganglion.
J Neurophysiol. 1994 May;71(5):1835-47
PMID: 8064351
-
Central trajectories of type II spiral ganglion cells from various cochlear regions in mice.
Hear Res. 1994 May;75(1-2):121-30
PMID: 8071139
-
Hair cell based amplification in the cochlea.
Curr Opin Neurobiol. 1994 Aug;4(4):503-8
PMID: 7812138
-
Endogenous firing patterns of murine spiral ganglion neurons.
J Neurophysiol. 1997 Mar;77(3):1294-305
PMID: 9084597