Otolith and canal integration on single vestibular neurons in cats

Department of Physiology, Tokyo Medical University, 6-1-1 Shinjuku, Shinjuku-ku, Tokyo, 160-8402, Japan.
Experimental Brain Research (Impact Factor: 2.04). 08/2005; 164(3):271-85. DOI: 10.1007/s00221-005-2341-7
Source: PubMed


In this review, based primarily on work from our laboratory, but related to previous studies, we summarize what is known about the convergence of vestibular afferent inputs onto single vestibular neurons activated by selective stimulation of individual vestibular nerve branches. Horizontal semicircular canal (HC), anterior semicircular canal (AC), posterior semicircular canal (PC), utricular (UT), and saccular (SAC) nerves were selectively stimulated in decerebrate cats. All recorded neurons were classified as either projection neurons, which consisted of vestibulospinal (VS), vestibulo-oculospinal (VOS), vestibulo-ocular (VO) neurons, or non-projection neurons, which we simply term "vestibular'' (V) neurons. The first three types could be successfully activated antidromically from oculomotor/trochlear nuclei and/or spinal cord, and the last type could not be activated antidromically from either site. A total of 1228 neurons were activated by stimulation of various nerve pair combinations. Convergent neurons were located in the caudoventral part of the lateral, the rostral part of the descending, and the medial vestibular nuclei. Otolith-activated vestibular neurons in the superior vestibular nucleus were extremely rare. A high percentage of neurons received excitatory inputs from two nerve pairs, a small percentage received reciprocal convergent inputs and even fewer received inhibitory inputs from both nerves. More than 30% of vestibular neurons received convergent inputs from vertical semicircular canal/otolith nerve pairs. In contrast, only half as many received convergent inputs from HC/otolith-nerve pairs, implying that convergent input from vertical semicircular canal and otolith-nerve pairs may play a more important role than that played by inputs from horizontal semicircular canal and otolith-nerve pairs. Convergent VS neurons projected through the ipsilateral lateral vestibulospinal tract (i-LVST) and the medial vestibulospinal tract (MVST). Almost all the VOS neurons projected through the MVST. Convergent neurons projecting to the oculomotor/trochlear nuclei were much fewer in number than those projecting to the spinal cord. Some of the convergent neurons that receive both canal and otolith input may contribute to the short-latency pathway of the vestibulocollic reflex. The functional significance of these convergences is discussed.

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    • "The primary output of the vestibular end organs is the vestibular nuclei in the brainstem. In particular, the medial vestibular nucleus (MVN) responds to stimulation of the horizontal semicircular canals (Uchino et al. 2005). The exact route by which vestibular information within the MVN is conveyed to the DTN and contributes to the HD signal is still under investigation. "
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    ABSTRACT: To maintain spatial orientation and guide navigation, an animal must have knowledge of its location and displacement of distance and direction from that location. Cells within the hippocampal formation and connected structures are spatially correlated to location and direction. Specifically, head direction (HD) cells discharge as a function of the directional heading of an animal, independent of their location or behavior. HD cells are found in many brain regions, but the classic circuit involved in generating, updating, and controlling their responses originates in the dorsal tegmental nucleus and projects serially to the lateral mammillary nucleus, anterior thalamic nuclei, and post-and parasubiculum and terminates in the entorhinal cortex. The HD signal is generated by self-movement cues, with the vestibular system playing a critical role. However, HD cells become strongly controlled by environmental cues, particularly visual landmarks. HD cells provide a continuous signal that an animal will use to guide its behavior and maintain orientation. Information provided by HD cells may be critical for generating the grid cell, but not for the place cell signal. Collectively, information from HD, place, and grid cells provide a complete representation of the animal's orientation in space.
    Space, Time and Memory in the Hippocampal Formation, 1 edited by D. Derdikman and J.J. Knierim, 01/2014: chapter 4: pages 24; Springer-Verlag Wien.
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    • "In rat, convergence of macular and canal inputs concern about 80% of tested vestibular neurons [3]. In cat, 1/3 of studied neurons receive convergent inputs from vertical canals and otoliths and 1/5 receive convergent inputs from horizontal canals and otoliths [4]. The anatomical convergence and functional complementarities between canals and otoliths raise questions on how spatial refinements of vestibular microcircuits at the origin of the vestibulo-ocular reflex (VOR) occur during development and adapt throughout lifespan. "
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    ABSTRACT: The vestibular organs consist of complementary sensors: the semicircular canals detect rotations while the otoliths detect linear accelerations, including the constant pull of gravity. Several fundamental questions remain on how the vestibular system would develop and/or adapt to prolonged changes in gravity such as during long-term space journey. How do vestibular reflexes develop if the appropriate assembly of otoliths and semi-circular canals is perturbed? The aim of present work was to evaluate the role of gravity sensing during ontogeny of the vestibular system. In otoconia-deficient mice (ied), gravity cannot be sensed and therefore maculo-ocular reflexes (MOR) were absent. While canals-related reflexes were present, the ied deficit also led to the abnormal spatial tuning of the horizontal angular canal-related VOR. To identify putative otolith-related critical periods, normal C57Bl/6J mice were subjected to 2G hypergravity by chronic centrifugation during different periods of development or adulthood (Adult-HG) and compared to non-centrifuged (control) C57Bl/6J mice. Mice exposed to hypergravity during development had completely normal vestibulo-ocular reflexes 6 months after end of centrifugation. Adult-HG mice all displayed major abnormalities in maculo-ocular reflexe one month after return to normal gravity. During the next 5 months, adaptation to normal gravity occurred in half of the individuals. In summary, genetic suppression of gravity sensing indicated that otolith-related signals might be necessary to ensure proper functioning of canal-related vestibular reflexes. On the other hand, exposure to hypergravity during development was not sufficient to modify durably motor behaviour. Hence, 2G centrifugation during development revealed no otolith-specific critical period.
    PLoS ONE 07/2012; 7(7):e40414. DOI:10.1371/journal.pone.0040414 · 3.23 Impact Factor
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    • "Sound-evoked saccular neurons project to and synapse on neurons in the ipsilateral vestibular nuclei and inhibitory neurons in the vestibular nuclei project ipsilaterally to spinal motoneurons and inhibit them (Uchino et al., 2005). In healthy subjects short tone bursts of 500 Hz of either high intensity ACS or moderate BCV result in a stimulus-locked short-latency inhibitory myogenic potential recorded by electrodes over tensed sternocleidomastoid muscles (SCM). "
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    ABSTRACT: This paper is focussed on one major aspect of compensation: the recent behavioural findings concerning oculomotor responses in human vestibular compensation and their possible implications for recovery after unilateral vestibular loss (UVL). New measurement techniques have provided new insights into how patients recover after UVL and have given clues for vestibular rehabilitation. Prior to this it has not been possible to quantify the level of function of all the peripheral vestibular sense organs. Now it is. By using vestibular-evoked myogenic potentials to measure utricular and saccular function and by new video head impulse testing to measure semicircular canal function to natural values of head accelerations. With these new video procedures it is now possible to measure both slow phase eye velocity and also saccades during natural head movements. The present evidence is that there is little or no recovery of slow phase eye velocity responses to natural head accelerations. It is doubtful as to whether the modest changes in slow phase eye velocity to small angular accelerations are functionally effective during compensation. On the other hand it is now clear that saccades can play a very important role in helping patients compensate and return to a normal lifestyle. Preliminary evidence suggests that different patterns of saccadic response may predict how well patients recover. It may be possible to train patients to produce more effective saccadic patterns in the first days after their unilateral loss. Some patients do learn new strategies, new behaviours, to conceal their inadequate VOR but when those strategies are prevented from operating by using passive, unpredictable, high acceleration natural head movements, as in the head impulse test, their vestibular loss can be demonstrated. It is those very strategies which the tests exclude, which may be the cause of their successful compensation.
    Frontiers in Neurology 02/2012; 3:21. DOI:10.3389/fneur.2012.00021
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