The development of the spiral ganglion was studied in steps sections of
81 human temporal bones.
By the 8th week, the spiral ganglion has already separated from the vestibular
ganglion. At 13 weeks two distinct populations are observed that correspond to
neuron and Schwann cells. At 15 weeks the spiral ganglion has increased its
distance from the cochlear duct and is surrounded by mesenchyme near the
scala tympani. At 14 weeks a gradual decrease in the nucleus-to-cell area ratio
was observed in spiral ganglion neurons that may reflect a morphological adaptation
to function. By the 23rd week the modiolus begins to ossify and the spiral
ganglion is surrounded by bony trabeculae.
The time course of spiral ganglion development follows that of the stria vascularis
and organ of Corti, although maturation changes are still observed in the
neuronal population even beyond 20 weeks

Anagnostopoulou, S.

Bibas, A.

Hornigold, R.

Liang, J.

Michaels, L.

Wright, A.

English

Via Medica Journals

Folia Morphol. Vol. 65, No. 2, pp. 140–144Copyright © 2006 Via MedicaISSN 0015–5659www.fm.viamedica.plO R I G I N A L   A R T I C L E140Address for correspondence: A. Bibas, 2 Nikitara Str, 154 51 Athens, Greece, tel: 0030 210 6775 600, e-mail: thanosbibas@hotmail.comThe development of the spiral ganglion in thehuman foetusA. Bibas1, R. Hornigold1, J. Liang1, L. Michaels1, S. Anagnostopoulou2, A. Wright11Institute of Laryngology and Otology, Royal Free and University College London Medical School, England2Department of Anatomy, National & Kapodistrian University of Athens, Greece[Received 6 January 2006; Revised 31 March 2006; Accepted 31 March 2006]The development of the spiral ganglion was studied in steps sections of81 human temporal bones.By the 8th week, the spiral ganglion has already separated from the vestibularganglion. At 13 weeks two distinct populations are observed that correspond toneuron and Schwann cells. At 15 weeks the spiral ganglion has increased itsdistance from the cochlear duct and is surrounded by mesenchyme near thescala tympani. At 14 weeks a gradual decrease in the nucleus-to-cell area ratiowas observed in spiral ganglion neurons that may reflect a morphological adap-tation to function. By the 23rd week the modiolus begins to ossify and the spiralganglion is surrounded by bony trabeculae.The time course of spiral ganglion development follows that of the stria vascu-laris and organ of Corti, although maturation changes are still observed in theneuronal population even beyond 20 weeks.Key words: spiral ganglion, development, human foetusINTRODUCTIONThe spiral ganglion is a population of bipolar cellssituated at the base of the bony spiral lamina. In thehuman adult cochlea it contains approximately35 000 neurons. Their peripheral processes synapsewith the hair cells of the organ of Corti, while theircentral processes form the cochlear nerve. Two dis-tinct populations of neurons have been identified,type I and type II. A third type of neuron, the inter-mediate cell, has also been described by Rosbe et al,with a cell area that significantly varies from type Iand type II neurons [13]. It is suggested that this isa subtype of the large type I cell.The development of the spiral ganglion has beenextensively described in small mammals [1, 11, 12].However, few studies have been published regardingits development in the human foetus, and these eitherinvolve a small number of temporal bones or concen-trate mainly on postnatal maturation [7, 14, 15]. Thepurpose of this paper is to present a comprehensivelight microscopy study covering consecutive steps inthe development of the human spiral ganglion.MATERIAL AND METHODSSections of human temporal bones ranging in agefrom 8 weeks of gestation to full term were exam-ined in this study. The material was derived from thetemporal bone collection of the Institute of Laryn-gology and Otology and obtained from perinataldeaths. All foetal specimens were decalcified, em-bedded and then cut horizontally, commencing atthe upper surface of the temporal bone. The em-bedding medium in the majority of cases was low-viscosity nitrocellulose, a substance related to celloi-din. In a small number of cases paraffin wax wasused. In the nitrocellulose-embedded material sec-tions had been cut at 20 µm thickness and everytenth section was mounted on glass slides andstained with haematoxylin and eosin. Paraffin waxsections were cut at 7 µm.141A. Bibas et al., Spiral ganglion developmentFrom 208 human foetuses 98 were initially se-lected. Inclusion criteria for the study included ab-sence of evidence of congenital disease in the med-ical history, a recorded age of gestation and/ora measured crown-rump length. During the studyspecimens that were observed to suffer from severeautolysis and were not suitable for any meaningfulobservations were excluded. Foetuses with obviouscongenital abnormality were equally excluded.Eighty-one temporal bones from 45 foetuses werefinally studied. The temporal bones of one child andfour adults were used as controls. In 41 foetuses theage was estimated using the crown-rump length. Inthe remainder the age was calculated from the firstday of the last normal menstruation as this appearedin the medical notes.RESULTSAt the end of the 8th week the acoustic ganglionhad already separated from the vestibular ganglion.Two large populations of neuroblasts could be dis-tinguished, a smaller one near the basal turn of thecochlear duct, and a relatively larger one near thedeveloping apical turn (Fig. 1A). Both were surround-ed by undifferentiated mesenchyme. The spiral gan-glion primordium in the basal turn was kidneyshaped. The primordium in the apical turns was morerounded in shape and two areas with different stain-ing properties could be distinguished in low magni-fication. There was a lighter staining area, which wasapposed to the developing cochlear duct, and a dark-er staining region that faced the developing internalauditory meatus (Fig. 1B). In the lighter stained areathere were very few cells and abundant neuroglia.In the darker staining area there was a cluster ofcells with round nuclei and staining variability. Schw-annoblasts and neuroblasts could not be identifiedmorphologically. By the end of the 11th week thespiral ganglion primordium of the apical turn hada spherical appearance and was beginning to sepa-rate into three different populations, each innervat-ing a different part of the developing cochlear duct(Fig. 1C). At the basal turn it had assumed a triangu-lar shape, with its apex towards the developing co-chlear duct (Fig. 1D). It was still difficult to differen-tiate between Schwann cells and neuroblasts.At 13 weeks the distance between the spiral gangli-on and the cochlear duct increased. The spiral gan-glion assumed a more oval shape with two process-es: a proximal one attached to the cochlear duct anda peripheral one forming the cochlear nerve (Fig. 2A).Schwann cells were clearly distinguished in theFigure 1. A. 8-week foetus (specimen C22). The cochlear duct has completed 1½ turns.CD — cochlear duct, SG — spiral ganglion; VIIIn — coclear nerve (× 25). B. Spiral ganglionprimordium at the apical turn of the developing cochlear duct (specimen C22); SG — spiralganglion, IAM — internal auditory meatus (× 50). C. 11-week foetus (specimen C11). Spiralganglion primordium branches off to innervate different parts of the developing cochlear duct(× 50); SG — spiral ganglion; CN — cochlear nerve; D. Spiral ganglion primordium has assumeda triangular shape in the basal turn (specimen C11); SG — spiral ganglion (× 100).142Folia Morphol., 2006, Vol. 65, No. 2central processes by their elongated light stained nu-cleus. In the spiral ganglion itself two distinct cellpopulations with different staining properties couldbe observed (Fig. 2B): cells with a lighter stained nu-cleus (neuron cells) and cells with a darker stainednucleus (Schwann cells).At 14 weeks Schwann cells appeared as dark elon-gated cells in the proximal process of the spiral gan-glion and as dark round satellite cells at the periph-ery of neuron cells (Fig. 2C, D). The nucleus-to-cyto-plasm ratio of neuron cells was just beginning todecrease and the cytoplasm looked clearer. Some ofthe neuron cells had developed a prominent nucleo-lus. By the 15th week the spiral ganglion had increasedits distance from the cochlear duct and was surround-ed by mesenchyme near the developing scala tym-pani. The number of Schwann cells in the centraland peripheral processes had increased considerably.The nucleus-to-cytoplasm ratio in neuron cells wasstill decreasing. At 18 weeks neuron cell cytoplasmstained mildly and was not as clear as in previoussections. The Schwann cells had now assumed a sick-le-cell shape, hugging the neuron cells (Fig. 3A, B).The spiral ganglion was now close to the scala tym-pani and still surrounded by mesenchyme.By the 23rd week, as the modiolus begins to ossi-fy, the spiral ganglion was surrounded by bony tra-beculae. The population of neuron cells seemed tohave decreased (Fig. 3C, D). In general, the neuroncells in the apical turn appeared larger than those inthe basal turn. By the end of the 25th week a furtherdecrease in the nucleus-to-cytoplasm ratio of neu-ron cells was observed. No major changes were ob-served after the 26th week.DISCUSSIONThe vestibulocochlear and geniculate ganglia areformed from a common ganglionic complex sur-rounded by mesenchyme [6]. The first sign of differ-entiation of the vestibular and cochlear ganglia isobserved as early as the 4th week [16]. As the foetalperiod commences, the spiral ganglion has alreadyseparated from the vestibular ganglion. Even thoughthe cellular population looks heterogeneous, it is stillnot possible to distinguish between Schwann cellsand neuron cells. The cochlear duct has already com-pleted one and a half turns and the initial ganglioncell population has branched off to innervate thebasal turn. As development progresses, ganglion cellclusters become separated to innervate the develop-ing cochlear duct in a progressive fashion as it con-tinues its coiling.The origin of the spiral ganglion primordium hasbeen a matter of considerable speculation and con-troversy. The two main theories are that it is of oto-cystic origin or that it is of neural crest origin [5],Figure 2. A. 13-week foetus (specimen T194). The spiral ganglion has assumed a more oval shape;SG — spiral ganglion, pp — proximal process, dp — distal process. (× 50). B. Higher magnificationof previous specimen with lighter (lc) and darker (dc) stained cells in the spiral ganglion (× 250).C. 14-week foetus (specimen C42); pp — peripheral process; dp — distal process (× 100). D. Highermagnification of previous specimen; NC — neuron cells, SC — Schwann cells (× 250).143A. Bibas et al., Spiral ganglion developmentalthough studies in birds postulate a double originfrom both structures [14]. However, no definite con-clusions can be drawn from our study. The proximi-ty of the spiral ganglion primordium to the develop-ing cochlear duct in the early stages of developmentmay be a strong indication in support of the otocys-tic theory. On the other hand, one cannot fail toobserve the increased presence of Schwann cellsalong the central auditory nerve projections throughthe foetal period of development. These cells maybe migrating towards the periphery, thus support-ing a neural crest origin, as suggested by other au-thors [14]. A study on the embryonic developmentof these structures is needed to draw more definiteconclusions.Another debate concerns whether hair cells dif-ferentiate before or after being contacted by nerveendings. With only a light microscopy study, such asours, it is difficult to shed light on this subject. Trans-mission electron microscopy has shown that affer-ent fibres can be observed as early as the 9th week,at a stage when it is impossible to distinguish withinthe otocyst the cells that are destined to becomehair cells [10].After the 14th week of development we observeda gradual decrease in the nucleus-to-cell area ratioin spiral ganglion neurons of all turns. This probablyreflects a morphological adaptation to function andhas also been observed in other human and animalstudies [2, 14].In our study spiral ganglion neurons reached theirfinal size at the end of the 18th week and neuron cellbodies in the apical turns were larger than in thebasal turn. This is consistent with the findings ofSanchez del Rey et al. [14]. Characteristics of thehuman neonatal spiral ganglion have been describedin a light and electron microscopic study of five tem-poral bones [8]. The prevalence of type II spiral gan-glion cells was found to be greater than in adults,constituting 24% of all neuronal cells in the middleturn and 26% in the basal turn, which decreasedwith increasing age. The study confirmed that thereis a clear differentiation between type I and II neu-rons in the human neonate. Ultrastructural studiesof mature human spiral ganglion cells have demon-strated that the diameter of large cell axons remainconsistently larger in the basal turn of the cochlearthan the middle and upper middle turns [9]. Thisseems to be a maturation rather than a developmen-tal process. It has been proposed that type II neu-rons are precursors to type I neurons [14] and thatthe maturation process occurs in an apical direction.The findings from our study would not dispute this,as neurons were consistently larger in the apical turnsthan in the basal turns, the opposite of the propor-tions found in adult studies.Figure 3 A. 18-week foetus (specimen T202); dp — distal process, pp — peripheral process;SV — scala vestibuli (× 50). B. Higher magnification of previous section. Nucleus-to-cytoplasm ra-tio has decreased considerably; g — neuron cell, sc — Schwann cell (× 250). C. 23-week foetus(specimen C306). Spiral ganglion in the apical turn (× 50); pp — peripheral process; ST — scalatympani. D. Previous specimen. Spiral ganglion in the basal turn; SG — spiral ganglion (× 50).144Folia Morphol., 2006, Vol. 65, No. 2In general the time course of spiral ganglion de-velopment follows that of the sensory epithelium andthe stria vascularis. At week 20 the neuron cells havealready reached their final size, while the organ ofCorti exhibits quite well developed fluid spaces andspecialised cells and the stria vascularis has formedcompletely [3]. This period is also the time by whichthe first responses to pure tone stimulation can bedetected in human foetuses [4]. However matura-tion changes are still observed in the neuronal pop-ulation even beyond 20 weeks. The population ofneuron cells seems to have decreased, while a fur-ther decrease in the nucleus-to-cytoplasm ratio ofneuron cells is observed by the end of the 25th week.CONCLUSIONA gradual decrease in the nucleus-to-cell arearatio was observed in spiral ganglion neurons in allturns. This is likely to reflect a morphological adap-tation to function and has also been observed inother human and animal studies. It has been pro-posed that type II neurons are precursors to type Ineurons and that the maturation process occurs inan apical direction. The findings from our studywould not dispute this. The time course of spiralganglion development follows that of the stria vas-cularis and organ of Corti, although maturationchanges are still observed in the neuronal popula-tion even beyond 20 weeks.ACKNOWLEDGEMENTSThis study was supported by the Alexander SOnassis Public Benefit Foundation (Hellenic Sectionof Scholarships and Research).REFERENCES1. Anniko M (1983) Early development and maturation ofthe spiral ganglion. Acta Otolaryngol, 95 (3–4): 263–276.2. Anniko M (1988) Maturation of inner ear ganglion cells.Morphometric analyses of cross-sectional areas. ORL,50: 103–109.3. Bibas A, Liang J, Michaels L, Wright A (2000) The de-velopment of the stria vascularis in the human foetus.Clin Otol, 25: 126–129.4. Birnholz JC, Benacerraf BR (1983) Development of hu-man fetal hearing. Science, 222: 516–518.5. Bruska M, Ulalowska-Blaszyk K, Wozniak W (2000)Neural crest contribution to the early development ofthe vestibulocochlear ganglion. Folia Morphol (Warsz),58: 243–246.6. Bruska M, Wozniak W (1994) Relation of the vestibu-lar ganglion to the otocyst and cochlear ganglion inhuman embryos during 5th and 6th week of develop-ment. Folia Morphol, 53: 85–93.7. Bruska M, Wozniak W (2000) The origin of cells of thecochlear ganglion in early human embryos. Folia Mor-phol, 59: 233–238.8. Chiong CM, Burgess BJ, Nadol JB Jr (1993) Postnatalmaturation of human spiral ganglion cells: light andelectron microscopic observations. Hear Res, 67 (1–2):211–219.9. Nadol JB Jr, Burgess BJ, Reisser C (1990) Morphomet-ric analysis of normal human spiral ganglion cells. AnnOtol Rhinol Laryngol, 99: 340–348.10. Pujol R, Lavigne-Rebillard M (1985) Early stages of in-nervation and sensory cell differentiation in the hu-man fetal Organ of Corti. Acta Otolaryngol (Stockh)Suppl, 421: 43–50.11. Romand MR, Romand R (1990) Development of spiralganglion cells in mammalian cochlea. J Electron Mi-crosc Tech, 15: 144–154.12. Romand R, Romand MR (1985) Qualitative and quan-titative observations of spiral ganglion developmentin the rat. Hear Res, 18: 111–120.13. Rosbe KW, Burgess BJ, Glynn RJ, Nadol JB (1996) Mor-phologic evidence for three cell types in the humanspiral ganglion. Hear Res, 93 (1–2): 120–127.14. Sanchez del Rey A, Sanchez-Fernandez JM, MartinezIbarguen A, Santaolalla Montoya F (1995) Morpho-logic and morphometric study of human spiral gan-glion development. Acta Otolaryngol (Stockh), 115:211–217.15. Ulatowska-Blaszyk K, Bruska M (1999) The cochlearganglion in human embryos of developmental stages18 and 19. Folia Morphol (Warsz), 58: 29–35.16. Wozniak W, Bruska M, Ulatowska-Blaszyk K, Skorze-wska A (1993) The vestibulocochlear ganglion in hu-man embryos at stage 13. Folia Morphol (Warsz), 52:97–107.

The development of the spiral ganglion in the human foetus

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The development of the spiral ganglion in the human foetus

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