Cerebellar Nodulectomy Impairs Spatial Memory of Vestibular and Optokinetic Stimulation in Rabbits

Barmack, Neal H.; Errico, P.; Ferraresi, Aldo; Fushiki, Hiroaki; Pettorossi, Vito Enrico; Yakhnitsa, Vadim

doi:10.1152/jn.00528.2001

Cited by 17 publications

(14 citation statements)

References 42 publications

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“…However, it should be noted that the cerebellar uvula and nodulus receives three different types of vestibular inputs: vestibular climbing fibers inputs from the contralateral inferior olive (Barmack and Shojaku 1995), and the primary and secondary vestibular mossy fiber inputs (Brodal and Høivik 1964; Korte and Mugnaini 1979; Carleton and Carpenter 1984; Epema et al 1985; Newlands et al 2002; Maklad and Fritzsch 2003a). They integrate information from these three sources and project back to VCN (Chan-Palay et al 1979; Epema et al 1985; Shojaku et al 1987; de Zeeuw and Berrebi 1996; Wylie et al 1999) to regulate spatial orientation, spatial memory, and reflexive eye movements (Ito et al 1970, 1971; Angelaki and Hess 1995; Barmack et al 2002; Cohen et al 2002). Our findings suggest that the primary afferent input is oppositely tuned from secondary vestibular mossy fibers inputs, but it is not clear how these oppositely tuned inputs are integrated in the vestibulocerebellum.…”

Section: Discussionmentioning

confidence: 99%

Development and organization of polarity-specific segregation of primary vestibular afferent fibers in mice

et al. 2010

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A striking feature of vestibular hair cells is the polarized arrangement of their stereocilia as the basis for their directional sensitivity. In mammals, each of the vestibular end organs is characterized by a distinct distribution of these polarized cells. We utilized the technique of post-fixation transganglionic neuronal tracing with fluorescent lipid soluble dyes in embryonic and postnatal mice to investigate whether these polarity characteristics correlate with the pattern of connections between the endorgans and their central targets; the vestibular nuclei and cerebellum. We found that the cerebellar and brainstem projections develop independently from each other and have a non-overlapping distribution of neurons and afferents from E11.5 on. In addition, we show that the vestibular fibers projecting to the cerebellum originate preferentially from the lateral half of the utricular macula and the medial half of the saccular macula. In contrast, the brainstem vestibular afferents originate primarily from the medial half of the utricular macula and the lateral half of the saccular macula. This indicates that the line of hair cell polarity reversal within the striola region segregates almost mutually exclusive central projections. A possible interpretation of this feature is that this macular organization provides an inhibitory side-loop through the cerebellum to produce synergistic tuning effects in the vestibular nuclei. The canal cristae project to the brainstem vestibular nuclei and cerebellum, but the projection to the vestibulocerebellum originates preferentially from the superior half of each of the cristae. The reason for this pattern is not clear, but it may compensate for unequal activation of crista hair cells or may be an evolutionary atavism reflecting a different polarity organization in ancestral vertebrate ears.

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Section: Discussionmentioning

confidence: 99%

Development and organization of polarity-specific segregation of primary vestibular afferent fibers in mice

et al. 2010

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“…When the head is in the initial orientation, the nystagmus is produced by the horizontal and medial rectus muscles. When the head is pitched, nystagmus in the same plane, and generated by the same stimulus, is produced by the vertical rectus and oblique muscles (Barmack et al 2002). This efficient reweighting indicates an important symmetry in the optokinetic system.…”

Section: Neural Organization Projects Vestibular Spacementioning

confidence: 93%

“…Their results show that reflex pathways can be reweighted so that the postural response to the same stimulus utilizes different movements of the torso and lower limbs to achieve compensation in the pointing direction of the head or gaze. An oculomotor example of symmetric reweighting appears in the modulation of optokinetic nystagmus by pitch rotation of the head (Barmack et al 2002). In these experiments it was shown that horizontal optokinetic stimulation generates horizontal nystagmus in the rabbit, regardless of the pitch orientation of the animal's head.…”

Section: Neural Organization Projects Vestibular Spacementioning

confidence: 94%

Spatial symmetries in vestibular projections to the uvula-nodulus

et al. 2007

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The discharge of secondary vestibular neurons relays the activity of the vestibular endorgans, occasioned by movements in three-dimensional physical space. At a slightly higher level of analysis, the discharge of each secondary vestibular neuron participates in a multifiber projection or pathway from primary afferents via the secondary neurons to another neuronal population. The logical organization of this projection determines whether characteristics of physical space are retained or lost. The logical structure of physical space is standardly expressed in terms of the mathematics of group theory. The logical organization of a projection can be compared to that of physical space by evaluating its symmetry group. The direct projection from the semicircular canal nerves via the vestibular nuclei to neck motor neurons has a full three-dimensional symmetry group, allowing it to maintain a three-dimensional coordinate frame. However, a projection may embed only a subgroup of the symmetry group of physical space, which incompletely mirrors the properties of physical space. The major visual and vestibular projections in the rabbit via the inferior olive to the uvula-nodulus carry three degrees of freedom-rotations about one vertical and two horizontal axes-but do not have full three dimensional symmetry. Instead, the vestibulo-olivo-nodular projection has symmetries corresponding to a product of two-dimensional vestibular and one-dimensional optokinetic spaces. This combination of projection symmetries provides the foundation for distinguishing horizontal from vertical rotations within a three dimensional space. In this study, we evaluate the symmetry group given by the physiological organization of the vestibulo-olivo-nodular projection. Although it acts on the same sets of elements and mirrors the rotations that occur in physical space, the physiological transformation group is distinct from the spatial group. We identify symmetries as products of physiological and spatial transformations. The symmetry group shapes the information the projection conveys to the uvula-nodulus; this shaping may depend on a physiological choice of generators, in the same way that function depends on the physiological choice of coordinates. We discuss the implications of the symmetry group for uvula-nodulus function, evolution, and functions of the vestibular system in general.

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“…Alternatively, it may be a consequence of nystagmus reorientation (Angelaki and Hess 1994). “Velocity dumping” can be altered without affecting nystagmus reorientation in nodulectomized rabbits (Barmack et al 2002) and monkeys (Wearne et al 1998). Consequently, spatiotemporal transformation may not require “velocity dumping,” at least for optokinetically evoked eye movements.…”

Section: Introductionmentioning

confidence: 99%

Head position modulates optokinetic nystagmus

Pettorossi¹,

Ferraresi²,

Botti³

et al. 2011

Exp Brain Res

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Orientation and movement relies on both visual and vestibular information mapped in separate coordinate systems. Here, we examine how coordinate systems interact to guide eye movements of rabbits. We exposed rabbits to continuous horizontal optokinetic stimulation (HOKS) at 5°/s to evoke horizontal eye movements, while they were statically or dynamically roll-tilted about the longitudinal axis. During monocular or binocular HOKS, when the rabbit was roll-tilted 30° onto the side of the eye stimulated in the posterior → anterior (P → A) direction, slow phase eye velocity (SPEV) increased by 3.5–5°/s. When the rabbit was roll-tilted 30° onto the side of the eye stimulated in the A → P direction, SPEV decreased to ~2.5°/s. We also tested the effect of roll-tilt after prolonged optokinetic stimulation had induced a negative optokinetic afternystagmus (OKAN II). In this condition, the SPEV occurred in the dark, “open loop.” Modulation of SPEV of OKAN II depended on the direction of the nystagmus and was consistent with that observed during “closed loop” HOKS. Dynamic roll-tilt influenced SPEV evoked by HOKS in a similar way. The amplitude and the phase of SPEV depended on the frequency of vestibular oscillation and on HOKS velocity. We conclude that the change in the linear acceleration of the gravity vector with respect to the head during roll-tilt modulates the gain of SPEV depending on its direction. This modulation improves gaze stability at different image retinal slip velocities caused by head roll-tilt during centric or eccentric head movement.

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Cerebellar Nodulectomy Impairs Spatial Memory of Vestibular and Optokinetic Stimulation in Rabbits

Cited by 17 publications

References 42 publications

Development and organization of polarity-specific segregation of primary vestibular afferent fibers in mice

Development and organization of polarity-specific segregation of primary vestibular afferent fibers in mice

Spatial symmetries in vestibular projections to the uvula-nodulus

Head position modulates optokinetic nystagmus

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