Frequency-Independent Synaptic Transmission Supports a Linear Vestibular Behavior

Bagnall, Martha W.; McElvain, Lauren E.; Faulstich, Michael E.; du, Sascha

doi:10.1016/j.neuron.2008.10.002

Cited by 76 publications

(102 citation statements)

References 59 publications

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“…However, saturation of postsynaptic receptors reduces the extent of changes in synaptic strength, allowing these synapses to provide a more reliable input to Purkinje cells (Wadiche and Jahr 2001;Foster et al 2002;Blitz et al 2004). For synapses in the vestibular nucleus, steady-state synaptic strength is independent of the frequency of sustained activation (Bagnall et al 2008), unlike most synapses, for which depression increases with elevated stimulus frequencies. This lack of plasticity likely reflects the interactions of multiple presynaptic mechanisms, and contributes to the linearity of vestibular reflexes by allowing this synapse to transmit synaptic charge that is linearly related to stimulus frequency.…”

Section: Short-term Presynaptic Plasticitymentioning

confidence: 99%

Short-Term Presynaptic Plasticity

Regehr

2012

Cold Spring Harbor Perspectives in Biology

428

358

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Section: Short-term Presynaptic Plasticitymentioning

confidence: 99%

Short-Term Presynaptic Plasticity

Regehr

2012

Cold Spring Harbor Perspectives in Biology

428

358

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“…This hypothesis was not experimentally verified on the network level, and in addition its enormous variation seems to prevent reliable information processing [13,14]. Here we experimentally demonstrate neuronal ultra-fast plasticity on a time scale of several milliseconds and its applications to advanced computational tasks.…”

Section: Introductionmentioning

confidence: 77%

Error correction and fast detectors implemented by ultrafast neuronal plasticity

2014

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We experimentally show that the neuron functions as a precise time-integrator, where the accumulated changes in neuronal response latencies, under complex and random stimulation patterns, are solely a function of a global quantity, the average time-lag between stimulations. In contrast, momentary leaps in the neuronal response latency follow trends of consecutive stimulations, indicating ultra-fast neuronal plasticity. On a circuit level, this ultra-fast neuronal plasticity phenomenon implements error-correction mechanisms and fast detectors for misplaced stimulations. Additionally, at moderate/high stimulation rates this phenomenon destabilizes/stabilizes a periodic neuronal activity disrupted by misplaced stimulations. I. INTRODUCTIONOn the network and circuit level, both synaptic and neuronal plasticity are present. These two distinct types of plasticity have different effects on the dynamics of a network [1,2]. On one hand, synaptic plasticity has been vastly researched, from the single neuron to the network level, specifically long and short-term plasticity. Shortterm synaptic plasticity reflects an increase (facilitation) and decrease (depression) in the probability of neurotransmitter release [3,4]. It affects the speed of synaptic signal transmission and can last from hundreds of milliseconds to seconds [3,5]. This phenomenon varies enormously depending on the neuronal and synaptic features as well as on the neuron's recent history of activity [6][7][8]. Neuronal plasticity, on the other hand, was examined mainly on the single neuron level [9,10], hence investigation of this phenomenon is still demanded.Short-term synaptic plasticity, in the form of facilitation and depression (FAD), is suggested to carry critical computational functions in neural circuits [1,11,12], thus one can hypothesize that neuronal plasticity carries similar computational functions. This hypothesis was not experimentally verified on the network level, and in addition its enormous variation seems to prevent reliable information processing [13,14]. Here we experimentally demonstrate neuronal ultra-fast plasticity on a time scale of several milliseconds and its applications to advanced computational tasks.

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“…One component of central vestibular neurons suspected of contributing to their nonlinear of behavior includes the expression of different voltage-dependent K ϩ conductances (Ris et al 2001), which make one type of neuron found in rodent slice preparations (type B) display nonlinear current-discharge relationships. However, other data, also in slice preparations, demonstrate remarkably linear input-output relationships for central vestibular neurons to current (du Lac and Lisberger 1995) and synaptic (Bagnall et al 2008) inputs. Potentially, local circuits may reconcile differences between findings in various preparations and may account for discrepancies in findings regarding linearity of responses in individual neurons (Pfanzelt et al 2008).…”

Section: Discussionmentioning

confidence: 94%

“…Most of these studies concerned the effect of frequency on the sensitivity and phase of responses of individual neurons and demonstrate a relatively flat relationship for frequencies between 0.1 and 2.0 Hz with an increasing phase lead relative to velocity as the frequency of rotation increases. Although studies of central vestibular neurons in vitro have addressed many aspects of response linearity (Bagnall et al 2008;du Lac and Lisberger 1995;Pfanzelt et al 2008), little systematic work has been done in vivo to understand how the magnitude of stimulation influences responses of central vestibular neurons. The linearity of the responses of central neurons over a range of rotational stimuli has not been directly addressed in normal, alert animals, although such responses have been reported in cats with unilateral vestibular lesions (Heskin-Sweezie et al 2007).…”

mentioning

confidence: 99%

Response Linearity of Alert Monkey Non-Eye Movement Vestibular Nucleus Neurons During Sinusoidal Yaw Rotation

Newlands

Lin²,

Wei³

2009

Journal of Neurophysiology

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Newlands SD, Lin N, Wei M. Response linearity of alert monkey non-eye movement vestibular nucleus neurons during sinusoidal yaw rotation. J Neurophysiol 102: 1388 -1397, 2009. First published June 24, 2009 doi:10.1152/jn.90914.2008. Vestibular afferents display linear responses over a range of amplitudes and frequencies, but comparable data for central vestibular neurons are lacking. To examine the effect of stimulus frequency and magnitude on the response sensitivity and linearity of non-eye movement central vestibular neurons, we recorded from the vestibular nuclei in awake rhesus macaques during sinusoidal yaw rotation at frequencies between 0.1 and 2 Hz and between 7.5 and 210°/s peak velocity. The dynamics of the neurons' responses across frequencies, while holding peak velocity constant, was consistent with previous studies. However, as the peak velocity was varied, while holding the frequency constant, neurons demonstrated lower sensitivities with increasing peak velocity, even at the lowest peak velocities tested. With increasing peak velocity, the proportion of neurons that silenced during a portion of the response increased. However, the decrease in sensitivity of these neurons with higher peak velocities of rotation was not due to increased silencing during the inhibitory portion of the cycle. Rather the neurons displayed peak firing rates that did not increase in proportion to head velocity as the peak velocity of rotation increased. These data suggest that, unlike vestibular afferents, the central vestibular neurons without eye movement sensitivity examined in this study do not follow linear systems principles even at low velocities. I N T R O D U C T I O NResponses of mammalian vestibular neurons, both peripheral and central, have been described for various stimulation paradigms. In vestibular afferent fibers, trade-off between the sensitivity of the cell's response and its linear range has been reported. Slow firing but sensitive irregular afferents effectively code acceleration only in the excitatory direction because once the firing rate of the neuron reaches inhibitory cutoff (rate of zero) the response of the cell remains zero (unchanged) with progressively more vigorous stimulation (Goldberg and Fernandez 1971b). Although the dynamics of vestibular afferent responses have been discussed extensively, less well understood is the impact of inhibitory cutoff and other nonlinearities in central vestibular neurons on the function of the vestibular system overall. Despite the known asymmetries in the primary afferent discharge, central mechanisms, especially the presence of a commissural system that provides informational redundancy in the vestibular nuclei, have been proposed to fill in the missing inhibitory information from one side of the midline with excitatory information from the other side (Abend 1978) to enable a linear output. Other authors have speculated on the possibilities of nonlinear processing in the central vestibular system ) and the role of population coding, which might provide...

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Frequency-Independent Synaptic Transmission Supports a Linear Vestibular Behavior

Cited by 76 publications

References 59 publications

Short-Term Presynaptic Plasticity

Short-Term Presynaptic Plasticity

Error correction and fast detectors implemented by ultrafast neuronal plasticity

Response Linearity of Alert Monkey Non-Eye Movement Vestibular Nucleus Neurons During Sinusoidal Yaw Rotation

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