The repetition timing of high frequency afferent stimulation drives the bidirectional plasticity at central synapses in the rat medial vestibular nuclei

Scarduzio, Mariangela; Panichi, Roberto; Pettorossi, Vito Enrico; Grassi, Silvia

doi:10.1016/j.neuroscience.2012.07.039

Cited by 22 publications

(19 citation statements)

References 63 publications

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“…Recordings were made in complete darkness from the same neurons before and after the application of a stimulation protocol previously shown to induce plasticity at the first central vestibular synapse in vitro (Fig. 2D lower inset) 24, 25 , and because the pulse rates fall within the physiological range of vestibular afferent firing rates 26 . Specifically, we first applied a short test sequence, consisting of pulse trains lasting 1 s, delivered at constant rates ranging from 25–300pps, to determine the baseline sensitivity of each neuron to different stimulation rates.…”

Section: Resultsmentioning

confidence: 99%

“…Further a recent report has shown that cerebellar-dependent mechanisms contribute to the induction of homeostatic plasticity in order to maintain an optimal working range of the vestibulo-ocular reflex 23 . On the other hand, in vitro studies have shown that repetitive stimulation of the vestibular nerve can alter the strength of afferent synapses onto the vestibular nuclei neurons over a time scale of minutes 24, 25 (Fig. 1B).…”

Section: Introductionmentioning

confidence: 99%

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Plasticity within excitatory and inhibitory pathways of the vestibulo-spinal circuitry guides changes in motor performance

Mitchell

Santina

Cullen

2017

Sci Rep

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Investigations of behaviors with well-characterized circuitry are required to understand how the brain learns new motor skills and ensures existing behaviors remain appropriately calibrated over time. Accordingly, here we recorded from neurons within different sites of the vestibulo-spinal circuitry of behaving macaque monkeys during temporally precise activation of vestibular afferents. Behaviorally relevant patterns of vestibular nerve activation generated a rapid and substantial decrease in the monosynaptic responses recorded at the first central stage of processing from neurons receiving direct input from vestibular afferents within minutes, as well as a decrease in the compensatory reflex response that lasted up to 8 hours. In contrast, afferent responses to this same stimulation remained constant, indicating that plasticity was not induced at the level of the periphery but rather at the afferent-central neuron synapse. Strikingly, the responses of neurons within indirect brainstem pathways also remained constant, even though the efficacy of their central input was significantly reduced. Taken together, our results show that rapid plasticity at the first central stage of vestibulo-spinal pathways can guide changes in motor performance, and that complementary plasticity on the same millisecond time scale within inhibitory vestibular nuclei networks contributes to ensuring a relatively robust behavioral output.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Plasticity within excitatory and inhibitory pathways of the vestibulo-spinal circuitry guides changes in motor performance

Mitchell

Santina

Cullen

2017

Sci Rep

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“…We demonstrated in this study that long-term VOR reduction is associated with a decrease in efficacy of the vestibular nerve synapses on MVNs, presumably through LTD-like mechanisms. It was shown that plasticity at this synapse can be induced by high-frequency stimulation of vestibular afferents, and that the direction of the plasticity is dependent on both developmental stage (Puyal et al, 2003) and stimulation pattern (Scarduzio et al, 2012) at basic potential (Idoux, 2015). Moreover, this plasticity is also dependent on the postsynaptic membrane potential (Pugh and Raman, 2006; McElvain et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Long-Lasting Visuo-Vestibular Mismatch in Freely-Behaving Mice Reduces the Vestibulo-Ocular Reflex and Leads to Neural Changes in the Direct Vestibular Pathway

Carcaud

Barros

Idoux

et al. 2017

eNeuro

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Calibration of the vestibulo-ocular reflex (VOR) depends on the presence of visual feedback. However, the cellular mechanisms associated with VOR modifications at the level of the brainstem remain largely unknown. A new protocol was designed to expose freely behaving mice to a visuo-vestibular mismatch during a 2-week period. This protocol induced a 50% reduction of the VOR. In vivo pharmacological experiments demonstrated that the VOR reduction depends on changes located outside the flocculus/paraflocculus complex. The cellular mechanisms associated with the VOR reduction were then studied in vitro on brainstem slices through a combination of vestibular afferent stimulation and patch-clamp recordings of central vestibular neurons. The evoked synaptic activity demonstrated that the efficacy of the synapses between vestibular afferents and central vestibular neurons was decreased. In addition, a long-term depression protocol failed to further decrease the synapse efficacy, suggesting that the VOR reduction might have occurred through depression-like mechanisms. Analysis of the intrinsic membrane properties of central vestibular neurons revealed that the synaptic changes were supplemented by a decrease in the spontaneous discharge and excitability of a subpopulation of neurons. Our results provide evidence that a long-lasting visuo-vestibular mismatch leads to changes in synaptic transmission and intrinsic properties of central vestibular neurons in the direct VOR pathway. Overall, these results open new avenues for future studies on visual and vestibular interactions conducted in vivo and in vitro.

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“…The fundamental computation performed by vestibular nerve synapses—wide-bandwidth linear filtering—could be produced, in principle, by overpowering calyceal synapses that ensure robust 1:1 postsynaptic responses to each presynaptic action potential. This arrangement, however, would preclude two critical operations of vestibular circuits: multisensory integration (Angelaki and Cullen, 2008; Sadeghi et al, 2012) and long-term, bidirectional experience dependent plasticity (McElvain et al, 2010; Menzies et al, 2010, Scarduzio et al, 2012). By distributing synaptic load across multiple independent release sites and operating well within the inherent dynamic limitations of cell biological machinery, vestibular nerve synapses satisfy systems requirements for wide bandwidth linear encoding, postsynaptic signal integration, and adaptive gain control.…”

Section: Discussionmentioning

confidence: 99%

Implementation of Linear Sensory Signaling via Multiple Coordinated Mechanisms at Central Vestibular Nerve Synapses

McElvain

Faulstich

Jeanne

et al. 2015

Neuron

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Summary Signal transfer in neural circuits is dynamically modified by the recent history of neuronal activity. Short-term plasticity endows synapses with nonlinear transmission properties, yet synapses in sensory and motor circuits are capable of signaling linearly over a wide range of presynaptic firing rates. How do such synapses achieve rate-invariant transmission despite history-dependent nonlinearities? Here, ultrastructural, biophysical, and computational analyses demonstrate that concerted molecular, anatomical, and physiological refinements are required for central vestibular nerve synapses to linearly transmit rate-coded sensory signals. Vestibular synapses operate in a physiological regime of steady-state depression imposed by tonic firing. Rate-invariant transmission relies on brief presynaptic action potentials that delimit calcium influx, large pools of rapidly mobilized vesicles, multiple low-probability release sites, robust postsynaptic receptor sensitivity, and efficient transmitter clearance. Broadband linear synaptic filtering of head motion signals is thus achieved by coordinately tuned synaptic machinery that maintains physiological operation within inherent cell biological limitations.

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The repetition timing of high frequency afferent stimulation drives the bidirectional plasticity at central synapses in the rat medial vestibular nuclei

Cited by 22 publications

References 63 publications

Plasticity within excitatory and inhibitory pathways of the vestibulo-spinal circuitry guides changes in motor performance

Plasticity within excitatory and inhibitory pathways of the vestibulo-spinal circuitry guides changes in motor performance

Long-Lasting Visuo-Vestibular Mismatch in Freely-Behaving Mice Reduces the Vestibulo-Ocular Reflex and Leads to Neural Changes in the Direct Vestibular Pathway

Implementation of Linear Sensory Signaling via Multiple Coordinated Mechanisms at Central Vestibular Nerve Synapses

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