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Plasticity of Scarpa's Ganglion Neurons as a Possible Basis for Functional Restoration within Vestibular Endorgans.

Travo C, Gaboyard-Niay S, Chabbert C - Front Neurol (2012)

Bottom Line: When co-cultured with vestibular epithelia, primary vestibular neurons were able to establish de novo contacts with hair cells.Under the present paradigm, these contacts displayed morphological features of immature synaptic contacts.Preliminary observations using co-cultures of adult rodents suggest that this reparative capacity remained in older mice although to a lesser extent.

View Article: PubMed Central - PubMed

Affiliation: INSERM U1051, Institute for Neurosciences Montpellier, France.

ABSTRACT
In a previous study, we observed spontaneous restoration of vestibular function in young adult rodents following excitotoxic injury of the neuronal connections within vestibular endorgans. The functional restoration was supported by a repair of synaptic contacts between hair cells and primary vestibular neurons. This process was observed in 2/3 of the animals studied and occurred within 5 days following the synaptic damage. To assess whether repair capacity is a fundamental trait of vestibular endorgans and to decipher the cellular mechanisms supporting such a repair process, we studied the neuronal regeneration and synaptogenesis in co-cultures of vestibular epithelia and Scarpa's ganglion from young and adult rodents. We demonstrate that, under specific culture conditions, primary vestibular neurons from young mice or rats exhibit robust ability to regenerate nervous processes. When co-cultured with vestibular epithelia, primary vestibular neurons were able to establish de novo contacts with hair cells. Under the present paradigm, these contacts displayed morphological features of immature synaptic contacts. Preliminary observations using co-cultures of adult rodents suggest that this reparative capacity remained in older mice although to a lesser extent. Identifying the basic mechanisms underlying the repair process may provide a basis for novel therapeutic strategies to restore mature and functional vestibular synaptic contacts following damage or loss.

No MeSH data available.


Related in: MedlinePlus

Details of synaptic contacts. In crista, electron microscopy highlights the different synaptic contacts formed de novo between hair cells and vestibular afferent terminals in 18 DIV co-cultures from P6 rats. Some fibers (green) contact multiple hair cells [(A), stars], while others contact only one hair cell forming a terminal that ensheathes the pre-synaptic type I hair cell [(B), I]. Bouton terminals (C,D) contact hair cells. Ribbons (white arrows) in hair cells face synaptic densities (white arrow heads). The fibers ensheating the type I-like hair cells (E–J) display typical features of mature and immature calyceal terminals. Fibers climb along the hair cell membrane facing ribbons (E–G), presenting some post-synaptic densities (F,G). Contacts with multiple (E,F) or single (G) ribbons were found. In these growing afferent fibers (H–J), typical small synaptic vesicles of immature calyceal innervations were observed in the newly formed terminals (black arrows) (I,J). Large granular vesicles (black arrow head) typical of peptidergic synaptic vesicles were also present in these growing calyceal terminals (I,J). Scale bars 5 μm in (A,B), 500 nm in (C,E,H), and 100 nm in (D,F,G,I,J).
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Figure 5: Details of synaptic contacts. In crista, electron microscopy highlights the different synaptic contacts formed de novo between hair cells and vestibular afferent terminals in 18 DIV co-cultures from P6 rats. Some fibers (green) contact multiple hair cells [(A), stars], while others contact only one hair cell forming a terminal that ensheathes the pre-synaptic type I hair cell [(B), I]. Bouton terminals (C,D) contact hair cells. Ribbons (white arrows) in hair cells face synaptic densities (white arrow heads). The fibers ensheating the type I-like hair cells (E–J) display typical features of mature and immature calyceal terminals. Fibers climb along the hair cell membrane facing ribbons (E–G), presenting some post-synaptic densities (F,G). Contacts with multiple (E,F) or single (G) ribbons were found. In these growing afferent fibers (H–J), typical small synaptic vesicles of immature calyceal innervations were observed in the newly formed terminals (black arrows) (I,J). Large granular vesicles (black arrow head) typical of peptidergic synaptic vesicles were also present in these growing calyceal terminals (I,J). Scale bars 5 μm in (A,B), 500 nm in (C,E,H), and 100 nm in (D,F,G,I,J).

Mentions: Subcellular characteristics of the newly formed cell-to-cell contacts were determined using electron microscopy (rats, n = 3). Bouton-type synaptic contacts were observed in crista (Figures 5A,C,D). Afferent terminals full of mitochondria often faced multiple ribbons located in hair cells, surrounded by clusters of mitochondria. Post-synaptic densities (PSD) were observed on membranes of afferent fibers facing pre-synaptic ribbons, confirming that newly formed synaptic contacts were established correctly. Calyx-type terminals were observed entering the sensory cell layer and enveloping type I hair cells (Figures 5B,E–J). Single and multiple ribbons were apposed to the calyx terminal membrane; some facing PSDs were observed on the nerve terminal membrane. Both bouton- and calyx-type terminals were full of mitochondria and vesicles. Two main types of vesicles were identified (Figures 5C,D,E–J): typical small synaptic vesicles and large granular vesicles (almost 100 nm length) filling both bouton-like terminal endings on type II hair cells and calyx-type climbing terminal afferents along type I hair cells. In summary, in this co-culture model, nerve endings arising from primary vestibular neurons entered vestibular sensory epithelia and contacted both type I and type II hair cells forming calyx- and bouton-type synaptic connections respectively. Several features of these newly formed synaptic contacts (expression of synaptophysin, presence of multiple ribbons, and post-synaptic accumulation of vesicles) suggest that at least up to 18 DIV, these contacts remained immature.


Plasticity of Scarpa's Ganglion Neurons as a Possible Basis for Functional Restoration within Vestibular Endorgans.

Travo C, Gaboyard-Niay S, Chabbert C - Front Neurol (2012)

Details of synaptic contacts. In crista, electron microscopy highlights the different synaptic contacts formed de novo between hair cells and vestibular afferent terminals in 18 DIV co-cultures from P6 rats. Some fibers (green) contact multiple hair cells [(A), stars], while others contact only one hair cell forming a terminal that ensheathes the pre-synaptic type I hair cell [(B), I]. Bouton terminals (C,D) contact hair cells. Ribbons (white arrows) in hair cells face synaptic densities (white arrow heads). The fibers ensheating the type I-like hair cells (E–J) display typical features of mature and immature calyceal terminals. Fibers climb along the hair cell membrane facing ribbons (E–G), presenting some post-synaptic densities (F,G). Contacts with multiple (E,F) or single (G) ribbons were found. In these growing afferent fibers (H–J), typical small synaptic vesicles of immature calyceal innervations were observed in the newly formed terminals (black arrows) (I,J). Large granular vesicles (black arrow head) typical of peptidergic synaptic vesicles were also present in these growing calyceal terminals (I,J). Scale bars 5 μm in (A,B), 500 nm in (C,E,H), and 100 nm in (D,F,G,I,J).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3368229&req=5

Figure 5: Details of synaptic contacts. In crista, electron microscopy highlights the different synaptic contacts formed de novo between hair cells and vestibular afferent terminals in 18 DIV co-cultures from P6 rats. Some fibers (green) contact multiple hair cells [(A), stars], while others contact only one hair cell forming a terminal that ensheathes the pre-synaptic type I hair cell [(B), I]. Bouton terminals (C,D) contact hair cells. Ribbons (white arrows) in hair cells face synaptic densities (white arrow heads). The fibers ensheating the type I-like hair cells (E–J) display typical features of mature and immature calyceal terminals. Fibers climb along the hair cell membrane facing ribbons (E–G), presenting some post-synaptic densities (F,G). Contacts with multiple (E,F) or single (G) ribbons were found. In these growing afferent fibers (H–J), typical small synaptic vesicles of immature calyceal innervations were observed in the newly formed terminals (black arrows) (I,J). Large granular vesicles (black arrow head) typical of peptidergic synaptic vesicles were also present in these growing calyceal terminals (I,J). Scale bars 5 μm in (A,B), 500 nm in (C,E,H), and 100 nm in (D,F,G,I,J).
Mentions: Subcellular characteristics of the newly formed cell-to-cell contacts were determined using electron microscopy (rats, n = 3). Bouton-type synaptic contacts were observed in crista (Figures 5A,C,D). Afferent terminals full of mitochondria often faced multiple ribbons located in hair cells, surrounded by clusters of mitochondria. Post-synaptic densities (PSD) were observed on membranes of afferent fibers facing pre-synaptic ribbons, confirming that newly formed synaptic contacts were established correctly. Calyx-type terminals were observed entering the sensory cell layer and enveloping type I hair cells (Figures 5B,E–J). Single and multiple ribbons were apposed to the calyx terminal membrane; some facing PSDs were observed on the nerve terminal membrane. Both bouton- and calyx-type terminals were full of mitochondria and vesicles. Two main types of vesicles were identified (Figures 5C,D,E–J): typical small synaptic vesicles and large granular vesicles (almost 100 nm length) filling both bouton-like terminal endings on type II hair cells and calyx-type climbing terminal afferents along type I hair cells. In summary, in this co-culture model, nerve endings arising from primary vestibular neurons entered vestibular sensory epithelia and contacted both type I and type II hair cells forming calyx- and bouton-type synaptic connections respectively. Several features of these newly formed synaptic contacts (expression of synaptophysin, presence of multiple ribbons, and post-synaptic accumulation of vesicles) suggest that at least up to 18 DIV, these contacts remained immature.

Bottom Line: When co-cultured with vestibular epithelia, primary vestibular neurons were able to establish de novo contacts with hair cells.Under the present paradigm, these contacts displayed morphological features of immature synaptic contacts.Preliminary observations using co-cultures of adult rodents suggest that this reparative capacity remained in older mice although to a lesser extent.

View Article: PubMed Central - PubMed

Affiliation: INSERM U1051, Institute for Neurosciences Montpellier, France.

ABSTRACT
In a previous study, we observed spontaneous restoration of vestibular function in young adult rodents following excitotoxic injury of the neuronal connections within vestibular endorgans. The functional restoration was supported by a repair of synaptic contacts between hair cells and primary vestibular neurons. This process was observed in 2/3 of the animals studied and occurred within 5 days following the synaptic damage. To assess whether repair capacity is a fundamental trait of vestibular endorgans and to decipher the cellular mechanisms supporting such a repair process, we studied the neuronal regeneration and synaptogenesis in co-cultures of vestibular epithelia and Scarpa's ganglion from young and adult rodents. We demonstrate that, under specific culture conditions, primary vestibular neurons from young mice or rats exhibit robust ability to regenerate nervous processes. When co-cultured with vestibular epithelia, primary vestibular neurons were able to establish de novo contacts with hair cells. Under the present paradigm, these contacts displayed morphological features of immature synaptic contacts. Preliminary observations using co-cultures of adult rodents suggest that this reparative capacity remained in older mice although to a lesser extent. Identifying the basic mechanisms underlying the repair process may provide a basis for novel therapeutic strategies to restore mature and functional vestibular synaptic contacts following damage or loss.

No MeSH data available.


Related in: MedlinePlus