Spatiotemporal pattern of action potential firing in developing inner hair cells of the mouse cochlea

Sendin, Gaston; Bourien, Jérôme; Rassendren, François; Puel, Jean–Luc; Nouvian, Régis

doi:10.1073/pnas.1319615111

Cited by 55 publications

(86 citation statements)

References 33 publications

(74 reference statements)

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“…These data suggest that from the end of the 1st postnatal week until hearing onset, IHCs fire brief trains of Ca 2+ spikes that lead to bursts of action potentials in SGNs, which then propagate through neurons in various auditory centers of the brain. The patterns of activity that precede (developmentally) this burst firing has been more difficult to establish -in vivo recordings from the MNTB in anesthetized rats showed limited activity (Tritsch et al 2010a), consistent with some in vitro studies (Brandt et al 2007;Tritsch and Bergles 2010), but counter to other reports of robust spontaneous firing of IHCs at this early developmental stage (Marcotti et al 2003a;Brandt et al 2007;Johnson et al 2011;Sendin et al 2014). In-vivo recordings from central auditory neurons in prehearing rodents have consistently failed to detect high rates of continuous firing such as that reported by these latter studies, suggesting that such activity may be confined to the cochlea at this age or that cochlear isolation in some cases enhances the excitability of IHCs.…”

Section: Developmental Changes In Spontaneous Activitysupporting

confidence: 57%

“…It has also been reported that IHCs in the apical and basal regions of cochlea exhibit different activities, with apical IHCs firing Ca 2+ spikes in bursts and basal IHCs firing continuously (P2-P5) (Johnson et al 2011). In contrast, a recent study found that both apical and basal IHCs exhibited burstfiring behavior (P1-P9) (Sendin et al 2014).…”

Section: Developmental Changes In Spontaneous Activitymentioning

confidence: 98%

“…While some studies have shown that IHCs sustain tonic firing, as noted above (Kros et al 1998;Marcotti et al 2003aMarcotti et al , 2003bMarcotti et al , 2004Brandt et al 2007), others reported that IHCs fire bursts of Ca 2+ spikes in the apex (Tritsch and Bergles 2010;Johnson et al 2011), or all along the length of the cochlea (Sendin et al 2014). Moreover, it has been shown that IHCs and SGNs exhibit burst activity in cochlear explants that have been maintained in vitro for several days (Tritsch et al 2010a), despite the absence of cholinergic axons.…”

Section: Introductionmentioning

confidence: 95%

“…For example, it has been shown that exogenous ATP can have excitatory (Tritsch et al 2007), inhibitory (Sendin et al 2014), or dual effects (Johnson et al 2011) on IHC firing, depending on the concentration and method of application used. In addition, one study reported that purinergic receptor inhibition increases the firing rate of IHCs (Johnson et al 2011).…”

Section: Introductionmentioning

confidence: 99%

“…In addition, one study reported that purinergic receptor inhibition increases the firing rate of IHCs (Johnson et al 2011). Moreover, the activity of IHCs recorded in whole mount preparations from the early postnatal cochlea varies from infrequent Ca 2+ spikes and bursting behavior (Brandt et al 2007;Tritsch and Bergles 2010) to steady firing (Marcotti et al 2003a;Sendin et al 2014).…”

Section: Introductionmentioning

confidence: 99%

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Spontaneous activity in the developing auditory system

Wang

Bergles

2014

Cell Tissue Res

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Spontaneous electrical activity is a common feature of sensory systems during early development. This sensory-independent neuronal activity has been implicated in promoting their survival and maturation, as well as growth and refinement of their projections to yield circuits that can rapidly extract information about the external world. Periodic bursts of action potentials occur in auditory neurons of mammals before hearing onset. This activity is induced by inner hair cells (IHCs) within the developing cochlea, which establish functional connections with spiral ganglion neurons (SGNs) several weeks before they are capable of detecting external sounds. During this pre-hearing period, IHCs fire periodic bursts of Ca(2+) action potentials that excite SGNs, triggering brief but intense periods of activity that pass through auditory centers of the brain. Although spontaneous activity requires input from IHCs, there is ongoing debate about whether IHCs are intrinsically active and their firing periodically interrupted by external inhibitory input (IHC-inhibition model), or are intrinsically silent and their firing periodically promoted by an external excitatory stimulus (IHC-excitation model). There is accumulating evidence that inner supporting cells in Kölliker's organ spontaneously release ATP during this time, which can induce bursts of Ca(2+) spikes in IHCs that recapitulate many features of auditory neuron activity observed in vivo. Nevertheless, the role of supporting cells in this process remains to be established in vivo. A greater understanding of the molecular mechanisms responsible for generating IHC activity in the developing cochlea will help reveal how these events contribute to the maturation of nascent auditory circuits.

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Section: Developmental Changes In Spontaneous Activitysupporting

confidence: 57%

Section: Developmental Changes In Spontaneous Activitymentioning

confidence: 98%

Section: Introductionmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Spontaneous activity in the developing auditory system

Wang

Bergles

2014

Cell Tissue Res

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Development of the innervation of the human inner ear

Pechriggl

Bitsche

Glueckert

et al. 2014

Developmental Neurobiology

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Studies on the formation of neuronal structures of the human cochlea are rare, presumptively, due to the difficult accessibility of specimens, so that most investigations are performed on mouse models. By means of immunohistochemical and transmission electron microscopic techniques, we investigated an uninterrupted series of unique specimens from gestational week 8 to week 12. We were able to demonstrate the presence of nerve fibers in the prosensory domain at gestational week 8, followed by afferent synaptogenesis at week 11. We identified PAX2 as an early marker for hair cell differentiation. Glutamine synthetase-positive peripheral glial cells occurred at the beginning of week 8. Transcription factor MAF B was used to demonstrate maturation of the spiral ganglion neurons. The early expression of tyrosine hydroxylase could be assessed. This study provides insights in the early assembly of the neural circuit and organization in humans.

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Talking back: Development of the olivocochlear efferent system

Frank

Goodrich

2018

WIREs Developmental Biology

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Developing sensory systems must coordinate the growth of neural circuitry spanning from receptors in the peripheral nervous system (PNS) to multilayered networks within the central nervous system (CNS). This breadth presents particular challenges, as nascent processes must navigate across the CNS-PNS boundary and coalesce into a tightly intermingled wiring pattern, thereby enabling reliable integration from the PNS to the CNS and back. In the auditory system, feedforward spiral ganglion neurons (SGNs) from the periphery collect sound information via tonotopically organized connections in the cochlea and transmit this information to the brainstem for processing via the VIII cranial nerve. In turn, feedback olivocochlear neurons (OCNs) housed in the auditory brainstem send projections into the periphery, also through the VIII nerve. OCNs are motor neuron-like efferent cells that influence auditory processing within the cochlea and protect against noise damage in adult animals. These aligned feedforward and feedback systems develop in parallel, with SGN central axons reaching the developing auditory brainstem around the same time that the OCN axons extend out toward the developing inner ear. Recent findings have begun to unravel the genetic and molecular mechanisms that guide OCN development, from their origins in a generic pool of motor neuron precursors to their specialized roles as modulators of cochlear activity. One recurrent theme is the importance of efferent-afferent interactions, as afferent SGNs guide OCNs to their final locations within the sensory epithelium, and efferent OCNs shape the activity of the developing auditory system. This article is categorized under: Nervous System Development > Vertebrates: Regional Development.

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Spatiotemporal pattern of action potential firing in developing inner hair cells of the mouse cochlea

Cited by 55 publications

References 33 publications

Spontaneous activity in the developing auditory system

Spontaneous activity in the developing auditory system

Development of the innervation of the human inner ear

Talking back: Development of the olivocochlear efferent system

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