Axonal projections of utricular afferents to the vestibular nuclei and the abducens nucleus in cats

Imagawa, Midori; Isu, Naoki; Sasaki, Mitsuyoshi; Endo, Kenji; Ikegami, Hitoshi; Uchino, Yuichi

doi:10.1016/0304-3940(95)11288-8

Cited by 65 publications

(62 citation statements)

References 13 publications

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“…The otolith-ocular pathways, however, have been shown to have a very different circuitry. Specifically, the utricule projections make monosynaptic and disynaptic excitatory connections to the ipsilateral abducens neurons and trisynaptic inhibitory connections to the contralateral abducens neurons (Imagawa et al 1995;Schwindt et al 1973;Uchino et al 1994Uchino et al , 1996Uchino et al , 1997. The saccular projections make no connections to the horizontal extraocular motoneurons.…”

Section: Click Activates Both Canal and Otolith Vor Pathwaysmentioning

confidence: 99%

Acoustic Clicks Activate both the Canal and Otolith Vestibulo-Ocular Reflex Pathways in Behaving Monkeys

Simpson

Tang

et al. 2009

JARO

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Acoustic activation of the vestibular system has been well documented in humans and animal models. In the past decade, sound-evoked myogenic potentials in the sternocleidomastoid muscle (cVEMP) and the extraocular muscles (oVEMP) have been extensively studied, and their potentials as new tests for vestibular function have been widely recognized. However, the extent to which sound activates the otolith and canal pathways remains controversial. In the present study, we examined this issue in a recently developed nonhuman primate model of acoustic activation of the vestibular system, i.e., sound-evoked vestibuloocular reflexes (VOR) in behaving monkeys. To determine whether the canal and otolith VOR pathways are activated by sound, we analyzed abducens neurons' responses to clicks that were delivered into either ear. The main finding was that clicks evoked short-latency excitatory responses in abducens neurons on both sides. The latencies of the two responses, however, were different. The mean latency of the contralateral and ipsilateral abducens neurons was 2.44±0.4 and 1.65±0.28 ms, respectively. A further analysis of the excitatory latencies, in combination with the known canal and otolith VOR pathways, suggests that the excitatory responses of the contralateral abducens neurons were mediated by the contralateral disynaptic VOR pathways that connect the lateral canal to the contralateral abducens neurons, and the excitatory responses of the ipsilateral abducens neurons were mediated by the ipsilateral monosynaptic VOR pathways that connect the utricle to the ipsilateral abducens neurons. These results provide new insights into the understanding of the neural basis for sound-evoked vestibular responses, which is essential for developing new tests for both canal and otolith functions in humans.

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Section: Click Activates Both Canal and Otolith Vor Pathwaysmentioning

confidence: 99%

Acoustic Clicks Activate both the Canal and Otolith Vestibulo-Ocular Reflex Pathways in Behaving Monkeys

Simpson

Tang

et al. 2009

JARO

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“…Electrical stimulation of both the utricle and saccule has been observed to induce extraocular muscle contractions and eye movements (Fluur and Mellstroem 1971;Isu et al 2000;Suzuki et al 1969). Utricular afferents principally project to the rostral part of the descending vestibular nucleus and ventral part of the lateral vestibular nucleus (Imagawa et al 1995). In cat, both the utricles and saccules project to abducens motoneurons (Uchino et al 1994, 1997aKushiro et al 2000).…”

Section: Possible Lateralization Of Otolith Pathologymentioning

confidence: 99%

“…In contrast, the LVOR is dominated by excitatory ipsilateral connections from the otoliths to ipsilateral abducens neurons with inhibitory connections to contralateral abducens neurons (Imagawa et al 1995;Schwindt et al 1973;Uchino et al 1994Uchino et al , 1996Uchino et al , 1997b. Most eyemovement related secondary vestibular neurons are activated not only by the semi-circular canals but also the otoliths (Angelaki et al 2001;Chen-Huang and McCrea 1999;King et al 2003;McConville et al 1996).…”

Section: Possible Lateralization Of Otolith Pathologymentioning

confidence: 99%

Effect of unilateral vestibular deafferentation on the initial human vestibulo-ocular reflex to surge translation

2006

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Transient whole-body surge (fore-aft) translation at 0.5 G peak acceleration was administered to six subjects with unilateral vestibular deafferentation (UVD), and eight age-matched controls. Subjects viewed eccentric targets to determine if linear vestibulo-ocular reflex (LVOR) asymmetry might lateralize otolith deficits. Eye rotation was measured using magnetic search coils. Immediately before surge, subjects viewed a luminous target 50 cm away, centered or displaced 10° horizontally or vertically. The target was extinguished during randomly directed surges. LVOR gain relative to ideal velocity in subjects with UVD for the contralesional horizontally eccentric target (0.59 ± 0.08, mean ± SEM) did not differ significantly from normal (0.50 ± 0.04), but gain for the ipsilesional eccentric target (0.35 ± 0.02) was significantly less than normal (0.48 ± 0.03, P < 0.05). Normal subjects had mean gain asymmetry for horizontally eccentric targets of 0.17 ± 0.03, but asymmetry in UVD was significantly increased to 0.35 ± 0.05 (P < 0.05). Four of six subjects with UVD had maximum gain asymmetry outside normal 95% confidence limits. Asymmetry did not correlate with UVD duration. Gain for 10° vertically eccentric targets averaged 0.38 ± 0.14 for subjects with UVD, insignificantly lower than the normal value of 0.75 ± 0.15 (P > 0.05). Surge LVOR latency was symmetrical in UVD, and did not differ significantly from normal. There was no significant difference in response between dark and visible target conditions until 200 ms after surge onset. Chronic human UVD, on average, significantly impairs the surge LVOR for horizontally eccentric targets placed ipsilesionally, but this asymmetry is small relative to interindividual variation.

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“…In contrast, the shortest latency excitatory utriculoabducens pathway is a weak ipsilateral projection, whereas the contralateral projections are at least trisynaptic and inhibitory (Schwindt et al, 1973;Uchino et al, 1994Uchino et al, , 1996, 1997; Imagawa et al, 1995). Because it is known that the large majority of type I PVP neurons make direct excitatory connections to the contralateral abducens (McCrea et al, 1987;Scudder and Fuchs, 1992), one must conclude that primary otolith afferents do not make monosynaptic projections to type I PVP neurons (Fig.…”

Section: Relationship Between Specific Cell Groups and Utriculoabducementioning

confidence: 99%

“…Finally, there is increasing evidence that the synaptic organization of the otolith-ocular and canal-ocular pathways is different. Whereas the shortest latency RVOR pathways are mediated dominantly by excitatory projections to the contralateral abducens, the shortest latency TrVOR pathways are instead excitatory to the ipsilateral abducens (Schwindt et al, 1973;Uchino et al, 1994Uchino et al, , 1996Uchino et al, , 1997Imagawa et al, 1995). These differences at both sensory and motor levels, as well as the existence of unique neuroanatomical connections, suggest that the sensorimotor processing of canal and otolith signals in the RVOR and TrVOR is at least partially distinct.…”

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confidence: 97%

Differential Sensorimotor Processing of Vestibulo-Ocular Signals during Rotation and Translation

2001

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Rotational and translational vestibulo-ocular reflexes (RVOR and TrVOR) function to maintain stable binocular fixation during head movements. Despite similar functional roles, differences in behavioral, neuroanatomical, and sensory afferent properties suggest that the sensorimotor processing may be partially distinct for the RVOR and TrVOR. To investigate the currently poorly understood neural correlates for the TrVOR, the activities of eye movement-sensitive neurons in the rostral vestibular nuclei were examined during pure translation and rotation under both stable gaze and suppression conditions. Two main conclusions were made. First, the 0.5 Hz firing rates of cells that carry both sensory head movement and motor-like signals during rotation were more strongly related to the oculomotor output than to the vestibular sensory signal during translation. Second, neurons the firing rates of which increased for ipsilaterally versus contralaterally directed eye movements (eye-ipsi and eye-contra cells, respectively) exhibited distinct dynamic properties during TrVOR suppression. Eye-ipsi neurons demonstrated relatively flat dynamics that was similar to that of the majority of vestibular-only neurons. In contrast, eye-contra cells were characterized by low-pass filter dynamics relative to linear acceleration and lower sensitivities than eye-ipsi cells. In fact, the main secondary eye-contra neuron in the disynaptic RVOR pathways (position-vestibular-pause cell) that exhibits a robust modulation during RVOR suppression did not modulate during TrVOR suppression. To explain these results, a simple model is proposed that is consistent with the known neuroanatomy and postulates differential projections of sensory canal and otolith signals onto eye-contra and eye-ipsi cells, respectively, within a shared premotor circuitry that generates the VORs.

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Axonal projections of utricular afferents to the vestibular nuclei and the abducens nucleus in cats

Cited by 65 publications

References 13 publications

Acoustic Clicks Activate both the Canal and Otolith Vestibulo-Ocular Reflex Pathways in Behaving Monkeys

Acoustic Clicks Activate both the Canal and Otolith Vestibulo-Ocular Reflex Pathways in Behaving Monkeys

Effect of unilateral vestibular deafferentation on the initial human vestibulo-ocular reflex to surge translation

Differential Sensorimotor Processing of Vestibulo-Ocular Signals during Rotation and Translation

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