Physiological properties of vestibular primary afferents that mediate motor learning and normal performance of the vestibulo-ocular reflex in monkeys

Bronte-Stewart, H. M.; Lisberger, S. G.

doi:10.1523/jneurosci.14-03-01290.1994

Cited by 30 publications

(17 citation statements)

References 33 publications

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“…The timecourse of the response to current steps varied across MVN neurons, suggesting that some of the differences in response dynamics in vivo could arise from intrinsic membrane properties. However, vestibular afferents also display a wide range of response dynamics (Bronte-Stewart and Lisberger 1994;Fernandez and Goldberg 1971), consistent with the possibility that response dynamics of MVN neurons in vivo could also be conferred by the signals present in their afferent inputs.…”

Section: Comparisons Of Mvn Neurons In Vivo and In Vitrosupporting

confidence: 59%

Membrane and firing properties of avian medial vestibular nucleus neurons in vitro

du¹,

Lisberger²

1995

J Comp Physiol A

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The intrinsic membrane and firing properties of medial vestibular nucleus (MVN) neurons were investigated in slices of the chick brainstem using intracellular recording and current injection. Avian MVN neurons fired spontaneous action potentials with very regular interspike intervals. The rapid repolarization of all action potentials was followed by an afterhyperpolarization. Intracellular injection of steps of hyperpolarizing current revealed both an inward rectification of the membrane potential during the step and a rebound depolarization following the offset of the step. In some neurons, the rebound depolarization resulted in bursts of action potentials. Steps of depolarizing current applied to spontaneously active neurons evoked increases in firing rate that were higher at the onset of the step than during the steady-state response. The relationship between current and firing rate was linear. The membrane and firing properties of avian MVN neurons were distributed continuously across the population of recorded neurons. These properties appear identical to those of rodent MVN neurons, suggesting that the composition and distribution of ion channels in the MVN neuronal membrane has been highly conserved across vertebrate species.Key words Chick 9 Brainstem 9 Slice 9 Intracellular recording 9 Action potential Abbreviations MVN medial vestibular nucleus 9 FOR vestibulo-ocular reflex 9 AHP after-hyperpolarization ' S. du Lac (l~) " S. G. Lisberger

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Section: Comparisons Of Mvn Neurons In Vivo and In Vitrosupporting

confidence: 59%

Membrane and firing properties of avian medial vestibular nucleus neurons in vitro

du¹,

Lisberger²

1995

J Comp Physiol A

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“…Prior analyses have suggested that the inputs to the VOR interneurons come from a diverse group of afferents (Highstein et al 1987) that are centered roughly in the middle of the distribution of dynamic response properties (Bronte-Stewart and Lisberger 1994;Minor and Goldberg 1991). Further, prior data suggest that the vestibular inputs to the unmodified pathways may have somewhat more phase lead compared with inputs to the modified pathways (Lisberger and Pavelko 1986;Lisberger et al 1994b).…”

Section: Sources Of Phase Shifts Of Ftns and Pvpsmentioning

confidence: 99%

Neural Substrate of Modified and Unmodified Pathways for Learning in Monkey Vestibuloocular Reflex

Ramachandran¹,

Lisberger²

2008

Journal of Neurophysiology

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Ramachandran R, Lisberger SG. Neural substrate of modified and unmodified pathways for learning in monkey vestibuloocular reflex. J Neurophysiol 100: 1868 -1878, 2008. First published July 30, 2008 doi:10.1152/jn.90498.2008. To understand how the brain learns, we need to identify the full neural circuit for a behavior; characterize how neural responses in the circuit change during behavioral learning; and understand the nature, location, and control of the cellular changes that are responsible for learning. This goal seems attainable for the vestibuloocular reflex (VOR), where the neural circuit basis for learning is already partially understood. The current hypothesis for VOR learning postulates cellular changes in the cerebellar cortex and the vestibular nucleus. It suggests that the brain stem contains two parallel pathways that have been modeled on the basis of extensive biological data as unmodified and modified VOR pathways with frequency-dependent internal gains and different time delays. We now show a correspondence between the responses of different groups of neurons in the vestibular nucleus and the signals emanating from the two pathways in the model. Floccular target neurons (FTNs) and position-vestibular-pause neurons (PVPs) were identified by their discharge during eye movements and by the presence or absence of inhibition by floccular stimulation. FTNs had response gains and phases that coincided with predictions for pathways that are modified in association with learning, whereas PVPs had responses in agreement with predictions for the unmodified pathways. The quantitative agreement of prior model predictions and new data supports the identity of FTNs and PVPs as brain stem interneurons in the modified and unmodified VOR pathways. Other aspects of the data make predictions about how vestibular inputs are transformed as they pass through the two pathways.

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“…Almost all VO neurons, for example, fire at shock strengths that only recruit irregular afferents (Goldberg et al 1994), yet these neurons are known to receive a significant regular input Boyle et al 1992). The interpretation of the effects of single shocks on the operation of multisynaptic pathways is even more difficult as it raises the need to specify the transformation between synaptic input and firing at several sites (Brontë-Stewart and Lisberger 1994).…”

Section: Central Mechanisms Central Terminations Of Vestibular-nerve mentioning

confidence: 99%

“…The second EPSP has a low threshold, but continues to grow as shock strength increases. Characteristics of regularly and irregularly discharging afferents, mammalian vestibular nerve High thresholds and small responses to the same galvanic stimuli a Goldberg and Fernández 1977;Yagi et al 1977;Baird et al 1988;Goldberg et al 1990a;Lysakowski et al 1995 b Goldberg andFernández 1971b;Yagi et al 1977;Fernández and Goldberg 1976b;Baird et al 1988;Goldberg et al 1990a;Lysakowski et al 1995 c Goldberg andFernández 1980;McCue andGuinan 1994 d Ezure et al 1983;Goldberg et al 1982Goldberg et al , 1984Goldberg et al , 1987Brontë-Stewart and Lisberger 1994 …”

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confidence: 99%

Afferent diversity and the organization of central vestibular pathways

2000

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This review considers whether the vestibular system includes separate populations of sensory axons innervating individual organs and giving rise to distinct central pathways. There is a variability in the discharge properties of afferents supplying each organ. Discharge regularity provides a marker for this diversity since fibers which differ in this way also differ in many other properties. Postspike recovery of excitability determines the discharge regularity of an afferent and its sensitivity to depolarizing inputs. Sensitivity is small in regularly discharging afferents and large in irregularly discharging afferents. The enhanced sensitivity of irregular fibers explains their larger responses to sensory inputs, to efferent activation, and to externally applied galvanic currents, but not their distinctive response dynamics. Morphophysiological studies show that regular and irregular afferents innervate overlapping regions of the vestibular nuclei. Intracellular recordings of EPSPs reveal that some secondary vestibular neurons receive a restricted input from regular or irregular afferents, but that most such neurons receive a mixed input from both kinds of afferents. Anodal currents delivered to the labyrinth can result in a selective and reversible silencing of irregular afferents. Such a functional ablation can provide estimates of the relative contributions of regular and irregular inputs to a central neuron's discharge. From such estimates it is concluded that secondary neurons need not resemble their afferent inputs in discharge regularity or response dynamics. Several suggestions are made as to the potentially distinctive contributions made by regular and irregular afferents: (1) Reflecting their response dynamics, regular and irregular afferents could compensate for differences in the dynamic loads of various reflexes or of individual reflexes in different parts of their frequency range; (2) The gating of irregular inputs to secondary VOR neurons could modify the operation of reflexes under varying behavioral circumstances; (3) Two-dimensional sensitivity can arise from the convergence onto secondary neurons of otolith inputs differing in their directional properties and response dynamics; (4) Calyx afferents have relatively low gains when compared with irregular dimorphic afferents. This could serve to expand the stimulus range over which the response of calyx afferents remains linear, while at the same time preserving the other features peculiar to irregular afferents. Among those features are phasic response dynamics and large responses to efferent activation; (5) Because of the convergence of several afferents onto each secondary neuron, information transmission to the latter depends on the gain of individual afferents, but not on their discharge regularity.

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Physiological properties of vestibular primary afferents that mediate motor learning and normal performance of the vestibulo-ocular reflex in monkeys

Cited by 30 publications

References 33 publications

Membrane and firing properties of avian medial vestibular nucleus neurons in vitro

Membrane and firing properties of avian medial vestibular nucleus neurons in vitro

Neural Substrate of Modified and Unmodified Pathways for Learning in Monkey Vestibuloocular Reflex

Afferent diversity and the organization of central vestibular pathways

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