Qualitative and quantitative observations of spiral ganglion development in the rat

doi:10.1016/0378-5955(85)90002-4

Hearing Research

Volume 18, Issue 2, May 1985, Pages 111-120

https://doi.org/10.1016/0378-5955(85)90002-4 Get rights and content

Abstract

The postnatal development of the spiral ganglion cells in the rat was studied from birth until the adult stage. At birth, a single population of ganglion cells is present. Some of them are surrounded by one or two layers of satellite cell processes. With maturation, the satellite cell processes increase in number around the cell body and its processes. At the end of the first postnatal week, two important events occur. The first is the appearance of myelin lamellae between the 4th and the 6th postnatal day in both ganglion cell processes, and between the 6th and the 8th day in the cell body. The second event is the appearance of a new type of cell (the Type II spiral ganglion cell) on the 6th to the 8th day postpartum. At this stage, the Type II cell is mainly characterized by densely packed neurofilamentous structures in the cytoplasm. Comparison between the myelination of the cell body and its processes reveals three main differences!

1.
(1) There is a time lag of approximately 2 days between the onset of myelination in the cell body and in its processes.
2.
(2) The kinetics of myelination are different in the cell processes and in the cell body. The myelination of the cell body starts slowly, whereas it is very fast in the processes. Later, the kinetics of myelination decrease in the processes, and increase in the cell body.
3.
(3) At all stages including the adult, the fibers have a myelin sheath composed of more lamellae than the cell body.

These observations are discussed with respect to development in other species.

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Cited by (48)

Reinvestigation of cochlear pathology in circling mice
2015, Neuroscience Letters
Citation Excerpt :
We also observed at least two types of cells: (1) larger cells containing a rich cytoplasm stained purple with a surrounding halo (filled arrow in Fig. 2) and (2) relatively smaller cells, stained light violet, without a surrounding halo (hollow arrow in Fig. 2). Most of the larger cells seemed to be Type I cells, but we were unsure as to whether the smaller cells without a surrounding halo were type II cells because other cell types such as satellite cells [17] or Schwann cells [6] are reported. As we could not distinguish type II cells from others with morphology base, we just counted cells separately (larger cells only vs. smaller cells and larger cells together).
The main causes of early hearing deficit in circling mice have been reported to be early degeneration of the organ of Corti and deterioration of spiral ganglion neurons. As an exact cochlear pathology is essential to explain our previous results regarding the auditory brainstem circuits of developing circling mice, we reinvestigated the cochlear pathology in developing circling mice (14, 22, and 38 days old).
It has been reported that the organ of Corti in circling mice completely degenerates as early as postnatal day (P) 21 and that circling mice are deaf by P18. Although we confirmed that circling mice were deaf at P15 and that hair bundles of outer hair cells were defective at P18, complete degeneration of the organ of Corti was not observed by P38 in circling mice. At P22, the type I cell-like spiral ganglion cell density in circling mice was reduced to 78% of that of control mice (ICR mice), but it was not significantly different from that of other control mice (heterozygous (+/cir) mice, littermates of circling mice) that could hear at P22.
Our data suggest that other factors, such as absence of neurotransmitter release from inner hair cells, should be considered to explain the early hearing deficit observed at P15 in circling mice.
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 Research
Citation Excerpt :
Although the two basic cell types of the spiral ganglion have distinctly different connections and roles, the morphological discrimination between them is not always easy. For example, in 6–8-day-old rats, type I and type II cells are practically indistinguishable from each other; and the morphological differences appear only at later stages of the development (Romand and Romand, 1985). Nevertheless, type I cells have been described as large, slightly elongated neurones whose cell bodies are enwrapped in a myelin sheath, whereas type II cells were considered as smaller, more spherical cells which do not possess a myelin cover.
The spiral ganglion accommodates the cell bodies of the acoustic nerve fibres connecting the hair cells to the central nervous system. As the ionic channels containing various voltage-gated K⁺ channel (Kv) subunits play pivotal roles in determining the functional properties and firing behaviour of the spiral ganglion cells (SGCs), every piece of information concerning the Kv expression of the SGCs is valuable. In the present work a comprehensive immunohistochemical analysis was performed to describe the expression of 9 Kv subunits in the guinea pig cochlea on traditional wax-embedded sections as well as employing a newly developed preparation that allowed confocal analysis, reconstruction of the three-dimensional appearance and precise morphological characterisation of the SGCs. Besides determining their Kv expression patterns, differences between type I and type II SGCs were sought. SGCs showed positivity for 8 out of the 9 Kv subunit-specific antibodies with varying intensity and proportion of the immunopositive cells; whereas no obvious Kv3.2 positivity could be noted. Type I and type II cells demonstrated similar expression patterns for all subunits tested, with the exception of Kv1.2, whose presence was confirmed in only 50% of the type II cells. Although the present findings suggest that type I and type II cells do not differ fundamentally in the Kv subunits they possess; they also imply that SGCs may not form a homogeneous cell population, and might provide explanation of the previously noted heterogeneity of the membrane properties of the SGCs.
Spatiotemporal patterns of neuronal programmed cell death during postnatal development of the gerbil cochlea
2005, Developmental Brain Research
During early postnatal development, afferent neurons of the cochlear (spiral) ganglion progressively refine their projections to auditory hair cells so that, by hearing onset, most cochlear nerve fibers innervate a single hearing receptor. One mechanism that might contribute to these changes in cochlear innervation is the programmed cell death (apoptosis) of developing neurons within the spiral ganglion. In the present study, we used the TUNEL method and morphological criteria to identify apoptotic cells within the spiral ganglion of the Mongolian gerbil during the first week of postnatal life when afferent projections to the cochlea are actively refined in this species. The locations of individual apoptotic spiral ganglion cells were mapped onto three-dimensional reconstructions of the entire ganglion for an age-graded series of gerbils to produce the first high-resolution, spatiotemporal maps of apoptotic ganglion cell death for the postnatal cochlea. We observed a significant increase in apoptosis in the spiral ganglion from postnatal day (P) 4 through P6. During this time, the most intense apoptotic activity occurred in regions of the spiral ganglion providing innervation to the lower middle and apical turns of the cochlea. The time course and regional variation of programmed cell death within the developing gerbil spiral ganglion are discussed in terms of the postnatal refinement of cochlear innervation and its possible functional significance for hearing in gerbils.
A-type potassium currents dominate repolarisation of neonatal rat primary auditory neurones in situ
2002, Neuroscience
Spiral ganglion neurones provide the afferent innervation to cochlear hair cells. Little is known of the molecular physiological processes associated with the differentiation of these neurones, which occurs up to and beyond hearing onset. We have identified novel A-type (inactivating) potassium currents in neonatal rat spiral ganglion neurones in situ, which have not previously been reported from the mammalian cochlea, presumably as a consequence of altered protein expression associated with other preparations. Under whole-cell voltage clamp, voltage steps activated both A-type and non-inactivating outward currents from around −55 mV. The amplitude of the A-type currents was dependent on the holding potential, with steady-state inactivation relieved at hyperpolarised potentials. At −60 mV (close to the resting potential in situ) the currents were approximately 30% enabled. The inactivation kinetics and the degree of inactivation varied between cells, suggesting heterogeneous expression of multiple inactivating currents. A-type currents provided around 60% of total conductance activated by depolarising voltage steps from the resting potential, and were very sensitive to bath-applied 4-aminopyridine (0.01–1 mM). Tetraethylammonium (0.1–30 mM) also blocked the majority of the A-type currents, and the non-inactivating outward current, but left residual fast inactivating A-type current. Under current clamp, neurones fired single tetrodotoxin-sensitive action potentials. 4-Aminopyridine relieved the A-type current mediated stabilisation of membrane potential, resulting in periodic small amplitude action potentials.
This study provides the first electrophysiological evidence for A-type potassium currents in neonatal spiral ganglion neurones and shows that these currents play an integral role in primary auditory neurone firing.
ATP-gated currents in rat primary auditory neurones in situ arise from a heteromultimetric P2X receptor subunit assembly
2002, Neuropharmacology
Spiral ganglion neurones provide the primary afferent innervation to sensory hair cells within the mammalian cochlea. Recent evidence suggests that their function may be modulated by purinergic signalling mechanisms, associated with release of adenosine 5′-triphosphate (ATP). Utilising a newly developed slice preparation of the neonatal rat cochlea, we have investigated the response of neurones in situ, to purinergic agonists and antagonists using whole-cell voltage clamp recordings. In cells identified as type I spiral ganglion neurones on the basis of morphology and voltage-dependent conductances, pressure-applied ATP, α,β-methyleneATP (α,β-meATP), 2-methylthioATP (2-MeSATP) and adenosine 5′-diphosphate (ADP) elicited a consistent phenotype of desensitising, inwardly rectifying current. The ATP-activated currents were reversibly blocked by the P2X receptor antagonists pyridoxalphosphate-6-azophenyl-2′,4′-disulphonic acid (PPADS, 10 μM), and 2′,3′-O-(2,4,6-trinitrophenyl)-ATP (TNP-ATP; IC₅₀ 407 nM). Neurones were more sensitive to ATP at low pH. The EC₅₀ value for ATP shifted from 18 μM at pH 7.3, to 1 μM at pH 6.3, with Hill coefficients of approximately 1. The results indicate that ATP-gated ion channels in spiral ganglion neurones arise from a specific heteromultimeric assembly of P2X receptor subunits which has no correspondence with present recombinant P2X receptor models.
Transient expression of P2X<inf>1</inf> receptor subunits of ATP-gated ion channels in the developing rat cochlea
2001, Developmental Brain Research
The expression pattern of the ATP-gated ion channel P2X₁ receptor subunit was studied in the developing rat cochlea by riboprobe in situ hybridisation and immunohistochemistry. Embryonic (E12, E14, E16 and E18) and postnatal (P0, P2, P4, P6, P10 and adult) rat cochleae were examined. Both mRNA and protein localisation techniques demonstrated comparable P2X₁ receptor expression from E16 until P6 but this expression was absent at later developmental stages. P2X₁ receptor mRNA expression was localised within the otic capsule and associated mesenchyme (from E16 to P6), spiral limbus (from P0 to P6) and within the spiral ligament adjacent to the insertion of Reissner’s membrane (from P2 to P6). P2X₁ receptor protein had a similar distribution based upon immunoperoxidase localisation. P2X₁ receptor-like immunoreactivity was detected in the otic capsule and the surrounding mesenchyme (from E16 to P6), spiral limbus (from P0) and epithelial cells of Reissner’s membrane (from P2 to P6). The spiral ganglion neurones showed the earliest P2X₁ receptor expression (from E16 to P6). This became associated with immunolabelling of their afferent neurite projections to the base of the developing inner and outer hair cells (observed from E18 and peaking at P2). Immunolabelling of the efferent nerve fibres of the intraganglionic spiral bundle (from E18 to P6) within the spiral ganglion was also observed. The results suggest that ATP-gated ion channels assembled from P2X₁ receptor subunits provide a signal transduction pathway for development of afferent and efferent innervation of the sensory hair cells and purinergic influence on cochlear morphogenesis.

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View full text

Qualitative and quantitative observations of spiral ganglion development in the rat

Abstract

Hearing Res.

Ultrastructural features of neurons and nerve fibres in the spiral ganglion of cats

J. Neurocytol.

Early development and maturation of the spiral ganglion

Acta Otolaryngol.

Development of cochlear function in the ear of the infant rat

J. Comp. Physiol. Psychol.

Development of the embryonic chick's stato acoustic ganglion

Acta Otolaryngol.

Hair-cell innervation by spiral ganglion cells in adult cat

Science

Development of hearing in the normal CBA-J mouse. Correlation of physiological observations with behavioural responses and with cochlear anatomy

Acta Otolaryngol.

A study of cochlear innervation patterns in cats and rats with the Golgi method and Nomarski optics

J. Comp. Neurol.

Maturation des potentiels cochléaires dans la période périnatale chez le Chat et chez le Cobaye

J. Physiol. (Paris)