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1 MacKay Institute of Communication and Neuroscience, School of Life Sciences, Keele University, Keele, Staffordshire ST5 5BG, UK
Email: m.g.evans{at}cns.keele.ac.uk
The cochlea of mammals has two types of hair cell, called inner and outer hair cells (IHCs and OHCs) according to their location on the cochlear spiral. The IHCs drive most of the auditory afferents, whereas the OHCs receive principally cholinergic efferent nerve fibres of the crossed olivocochlear bundle. This efferent innervation probably acts to control the OHCs in their role as cellular amplifiers of the travelling wave (produced by sound) on the cochlea's basilar membrane. But how does this pattern of innervation arise? During cochlear development in neonatal rats and mice, IHCs also receive efferent nerve fibres for a number of days prior to the onset of hearing at about 2 weeks of age. At this developmental stage, therefore, the mammalian IHC receives both afferent and efferent nerve fibres, a situation common in hair cells of lower vertebrates such as frogs and turtles. The efferent nerves reach the OHCs from about the beginning of the second postnatal week, thereby establishing the mature pattern of cochlear efferent innervation.
An investigation of this transient efferent innervation of rat inner hair cells in this issue of The Journal of Physiology has provided a rather unexpected boost towards the characterization of the cholinergic efferent synapse of the mammalian cochlea (Goutman et al. 2005). Using an excised preparation of the apical turn of the neonatal rat cochlea, Goutman et al. managed to electrically stimulate the efferent nerve fibres and record the inhibitory postsynaptic currents (IPSCs) from the IHCs. Single electrical shocks to the efferents elicited IPSCs but with a high failure rate, and a quantal analysis of the IPSC amplitudes indicated a low probability of release of synaptic vesicles from the efferent terminals. At –60 mV, stimulation evoked biphasic currents, reminiscent of previously reported responses in immature IHCs (Glowatzki & Fuchs, 2000) and mature OHCs (Evans, 1996; Blanchet et al. 1996), comprising a fast AChR current followed by a calcium-activated potassium (SK) current. When shocks were delivered in pairs, the IPSCs showed facilitation, meaning that the second shock was larger than the first by an amount that depended critically on the intershock interval. Analysis of the facilitated IPSCs indicated that the probability of release had increased.
Both the high failure rate and the pronounced facilitation were found in an earlier study of the turtle cochlea (Art et al. 1984), suggesting that the hair-cell efferent synapse shows remarkable conservation. As deduced in this earlier study, the first postsynaptic event is in fact an excitatory potential as AChRs open, producing inhibition as the calcium-activated potassium current is activated by calcium entering through the receptor. It has taken about 20 years to successfully repeat this type of experiment in the mammal. Key to this success has been the establishment of a viable preparation of the excised apical turn of the cochlea that enables stable recordings to be made while providing good access to the hair cells. This experimental approach should now be taken to investigate the OHC efferent synapse in hearing animals, and it will be interesting to see what is found.
There is good evidence that synaptic inhibition at both OHCs and IHCs is mediated by 
9/10 AChRs. Apart from its rather unusual pharmacology, the key feature of this receptor (as reported in immature IHCs) is its high permeability to calcium and its sensitivity to calcium, being potentiated in low external calcium and blocked in the millimolar range (Gomez-Casati et al. 2005 in this issue of The Journal of Physiology). Thus there appear to be two distinct calcium binding sites on the receptor. A similar calcium sensitivity has also been found for ACh-sensitive currents in neonatal IHCs (Marcotti et al. 2004).
There is still debate about the role of the efferent system in cochlear physiology, and naturally it centres on the OHC efferent synapse. Putting that to one side, what is the role of this developmentally transient IHC efferent synapse? As discussed by Goutam et al. (2005), it might play a role in regulating immature IHC spiking activity, which in turn could be important in establishing the mature pattern of innervation and function in the developing auditory pathway (see also Marcotti et al. 2004). In relation to this, it is clear that efferent stimulation at frequencies where facilitation occurs results in IHC hyperpolarization and a reduction in the number of spikes evoked during current injection (Goutman et al. 2005). This means that cochlear efferents have to be driven above a few hertz to exert a measurable affect on spiking rate, in accord with the classical work on cochlear efferent inhibition in mammals.
The picture that emerges is of a dynamic and plastic IHC efferent synapse. At present a specific role for the IHC efferents is still a matter of speculation, but in view of the recent progress it is likely that new data and ideas are not far off. The cochlear efferents appear to have a number of roles, not only in controlling cochlear output via an influence on the OHCs and thereby on cochlear mechanics, but also in aiding cochlear development.
References
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Blanchet
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Evans MG (1996). J Physiol 491, 563–578.[Medline]
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288, 2366–2368.
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