Chapter 2 Vestibular projections to the spinal cord: the morphology of single vestibulospinal axons

doi:10.1016/S0079-6123(08)64488-X

Progress in Brain Research

Volume 76, 1988, Pages 17-27

https://doi.org/10.1016/S0079-6123(08)64488-X Get rights and content

The three-dimensional distribution of LVST and MVST axons was examined in the cat cervical spinal cord using an intra-axonal staining method. LVST and MVST axons were electrophysiologically identified by their responses to stimulation of the vestibular nucleus, bilateral vestibular primary afferents, the LVST and the MVST were stained with injection of HRP. The axonal trajectory was reconstructed from serial histological sections. LVST axons were found to have multiple axon collaterals in the cervical cord. The maximum number of the identified collaterals for one neuron was 7. These collaterals were observed in either LVST axons terminating at the cervical cord or those projecting below Th2. The rostro-caudal extension of terminals for each collateral was very restricted (mean = 760 μm) and much narrower than intercollateral intervals (mean = 1470 μm). In the gray matter, collaterals ramified successively, pursued a delta-like path, and terminated mainly in lamina VIII and in the medial part of lamina VII and many boutons made apparent contact with the cell bodies and the proximal dendrites of motoneurons in the ventromedial nucleus. Some terminals were also distributed to the ventrolateral part of lamina VII adjacent to lamina IX. One group of LVST axons projected to lamina IX in the lateral ventral horn and terminated on large neurons there, probably motoneurons of forelimb muscles. MVST axons had one to seven axon collaterals at C1–C3 within the range of the stained axon. Stem axons ran in the ventromedial funiculus and primary collaterals arose from them at right angles. Each collateral had a very nar-row rostrocaudal spread as in LVST axons. Terminals were distributed in laminae VIII and IX, including the ventromedial nucleus, the spinal accessory nucleus, and the commissural nucleus. Many terminals seemed to make contact with retrogradely labelled motoneurons of neck muscles. Both crossed and uncrossed MVST axons had these characteristics.

References (43)

C. Abzug et al.
Branching of individual lateral vestibulospinal axons at different spinal cord levels
Brain Res.
(1973)
T. Akaike
Neuronal organization of the vestibulospinal system in the cat
Brain Res.
(1983)
M. Aoyama et al.
Convergent effects from the bilateral vestibulospinal tracts on spinal interneurons
Brain Res.
(1971)
G. Ten Bruggencate et al.
Interaction between the vestibulospinal tract, contralateral flexor reflex afferents and la afferents
Brain Res.
(1969)
T. Futami et al.
Spinal axon collaterals of corticospinal neurons identified by intracellu-lar injection of horseradish peroxidase
Brain Res.
(1979)
Y. Shinoda et al.
Divergent projection of individual corticospinal axons to motoneu-rons of multiple muscles in the monkey
Neurosci. Lett.
(1981)
Y. Shinoda et al.
Morphology of physiologically identified rubrospinal axons in the spinal cord of the cat
Brain Res.
(1982)
C. Abzug et al.
Cervical branching of lumbar vestibulospinal axons
J. Physiol. London
(1974)
S. Grillner et al.
The vestibulospinal tract. Effects on alpha-motoneurones in the lumbo-sacral spinal cord in the cat.
Exp. Brain Res.
(1970)
P.J. Harrison et al.
Lamina VIII interneurones interposed in crossed reflex pathways in the cat
J. Physiol. London
(1986)

E. Hauglie-Hanssen

Intrinsic neuronal organization of the vestibular nuclear complex in the cat. A Golgi study.

Ergeb. Anal. Entw. Gesch.

(1968)

T. Hongo et al.

The vestibulospinal tract: crossed and uncrossed effects in hindlimb motoneurones in the cat

Exp. Brain Res.

(1975)

H. Hultborn et al.

Convergence in the reciprocal la inhibitory pathway of excitation from descending pathways and inhibition from motor axon collaterals

Acta Physiol. Scand.

(1972)

H. Hultborn et al.

Convergence on interneurones mediating the reciprocal la inhibition of motoneurones. III. Effects from supraspinal pathways.

Acta Physiol. Scand.

(1976)

E. Jankowska et al.

Morphology of interneurones mediating la reciprocal inhibition of motoneurones in the spinal cord of the cat

J. Physiol. London

(1972)

N. Kawai et al.

Postsynaptic influences on the vestibular non-Deiters' nuclei from primary vestibular nerve

Exp. Brain Res.

(1969)

S. Lund et al.

Descending pathways with monosynaptic action on motoneurones

Experienlia

(1965)

S. Lund et al.

Monosynaptic excitation of alpha motoneurones from supraspinal structures in the cat

Acta Physiol. Scand.

(1968)

M. Maeda et al.

Labyrinthine influence on cat forelimb motoneurons

Exp. Brain Res.

(1975)

MannenH.

Arborisations dendritiques étude topo-graphique et quantitative dans le noyau vestibulaire du chat

Arch. Ital. Biol

(1965)

R. Nyberg-Hansen

Origin and termination of fibers from the vestibular nuclei descending in the medial longitudinal fasciculus. An experimental study with silver impregnation methods in the cat.

J. Neurol.

(1964)

Cited by (41)

6.20 - Task-Specific Differentiation of Central Vestibular Neurons and Plasticity During Vestibular Compensation
2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition
The vestibular system provides the sensorimotor transformation responsible for gaze stabilization and postural control and sends information about self-generated and externally applied movements to thalamic and cortical pathways. Neurons located in the four vestibular nuclei of vertebrates encode different aspects of head velocity together with eye/neck motion parameters and can be divided into functional subgroups based on their contributions to specific motor behaviors. The functional significance of the integration of vestibular signals with other inputs in different subsets of neurons during task-specific behaviors and their role in vestibular compensation are presented.
6.23 - Vestibulo-Spinal Pathways in Tetrapods
2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition
The vestibulospinal system provides the spinal motor circuits for head/neck and limb movements and body posture with rapid reflex adjustments to maintain equilibrium and stability. The continuous excitatory drive of descending vestibular pathways, called tonus, enhances reactive responses to perturbations of the normal posture. A striking observation in understanding the functional organization of this sensory-motor system is both that the driving sensory input can be dynamically modified by the behavioral context in which the sensation is made and that it remains able to quickly respond to an external force during self-generated head movements.
Vestibulospinal contributions to mammalian locomotion
2019, Current Opinion in Physiology
Citation Excerpt :
In primates, however, LVST-neurons do not appear to have brainstem collaterals [18]. Individual LVST axons have putative synaptic contacts through large portions of the ventral spinal cord, can collateralise at several spinal levels ([19]; Figure 1a) and can innervate multiple extensor motor neuron pools [9]. In mice, LVST axons are found throughout the ventral grey matter [9,20,21], with dense projections around both the lateral and medial motor columns (the location of limb and axial motor neurons, respectively).
The basic mammalian locomotor pattern is generated by spinal circuits which must maintain enough output flexibility to sustain locomotion in an ever-changing environment. Lateral vestibulospinal tract (LVST) neurons receive multimodal sensory feedback regarding ongoing movement, as well as input from the forebrain and cerebellum, and send dense projections to multiple areas of the spinal cord. Traditionally, LVST-neurons have been implicated in the generation of reflexes that maintain upright posture, but they may also have an underappreciated role in the generation of normal locomotor movements. Here, we review anatomical data regarding the inputs, projection pathways and spinal targets of LVST-neurons and discuss evidence from both animal and human studies around their potential role in the modification of locomotor patterns in mammals.
Physiology of central pathways
2016, Handbook of Clinical Neurology
Citation Excerpt :
VO neurons in the VN project to the cervical spinal cord and are thought to mediate the VCR pathway (Fig. 2.5) (Wilson et al., 1990; Boyle, 1993; Boyle et al., 1996; Gdowski and McCrea, 1999). Additionally, projections from vestibulospinal axons to both the cervical and/or lumbar levels of the spinal cord (Abzug et al., 1974; Rapoport et al., 1977; Shinoda et al., 1988) coordinate different parts of the musculature, for example, the neck and axial muscles during head movement to ensure stable posture. Similar to the VOR, the most direct pathway connecting the vestibular nerve and spinal cord motoneurons is a three-neuron arc.
The relative simplicity of the neural circuits that mediate vestibular reflexes is well suited for linking systems and cellular levels of analyses. Notably, a distinctive feature of the vestibular system is that neurons at the first central stage of sensory processing in the vestibular nuclei are premotor neurons; the same neurons that receive vestibular-nerve input also send direct projections to motor pathways. For example, the simplicity of the three-neuron pathway that mediates the vestibulo-ocular reflex leads to the generation of compensatory eye movements within ~ 5 ms of a head movement. Similarly, relatively direct pathways between the labyrinth and spinal cord control vestibulospinal reflexes. A second distinctive feature of the vestibular system is that the first stage of central processing is strongly multimodal. This is because the vestibular nuclei receive inputs from a wide range of cortical, cerebellar, and other brainstem structures in addition to direct inputs from the vestibular nerve. Recent studies in alert animals have established how extravestibular signals shape these “simple” reflexes to meet the needs of current behavioral goal. Moreover, multimodal interactions at higher levels, such as the vestibular cerebellum, thalamus, and cortex, play a vital role in ensuring accurate self-motion and spatial orientation perception.
Multisensory Signaling Shapes Vestibulo-Motor Circuit Specificity
2015, Cell
Citation Excerpt :
In the vestibular system, one central sensory organ in the inner ear monitors linear and rotational acceleration and provides input to the vestibular nucleus of the brainstem (Angelaki and Cullen, 2008; Brodal and Pompeiano, 1957). Descending vestibulo-spinal projection neurons transmit this information to spinal circuits to provide postural stability (Grillner et al., 1970; Lund and Pompeiano, 1968; Shinoda et al., 1988; Wilson and Yoshida, 1968). The somatosensory system represents a complementary signaling system in which sense organs are distributed throughout the entire body (Abraira and Ginty, 2013; Brown, 1981; Matthews, 1981).
The ability to continuously adjust posture and balance is necessary for reliable motor behavior. Vestibular and proprioceptive systems influence postural adjustments during movement by signaling functionally complementary sensory information. Using viral tracing and mouse genetics, we reveal two patterns of synaptic specificity between brainstem vestibular neurons and spinal motor neurons, established through distinct mechanisms. First, vestibular input targets preferentially extensor over flexor motor pools, a pattern established by developmental refinement in part controlled by vestibular signaling. Second, vestibular input targets slow-twitch over fast motor neuron subtypes within extensor pools, while proprioceptors exhibit inversely correlated connectivity profiles. Genetic manipulations affecting the functionality of proprioceptive feedback circuits lead to adjustments in vestibular input to motor neuron subtypes counterbalancing the imposed changes, without changing the sparse vestibular input to flexor pools. Thus, two sensory signaling systems interact to establish complementary synaptic input patterns to the final site of motor output processing.
Differences between otolith- and semicircular canal-activated neural circuitry in the vestibular system
2011, Neuroscience Research
Citation Excerpt :
In this set-up, the interneurons of the vestibular nuclei play an important role as a sensory motor terminal that drives motor neurons in the spinal cord (Wilson and Maeda, 1974; Rapoport et al., 1977a,b; Fukushima et al., 1979; Wilson and Melvill Jones, 1979). Similar to the vestibulo-oculomotor system, the vestibular nuclei interneurons are classified as vestibulo-collic (VC) and VOC neurons, with or without ascending axon collaterals to the oculomotor nuclei, respectively (Wilson and Maeda, 1974; Rapoport et al., 1977a,b; Wilson et al., 1979; Uchino and Hirai, 1984; Isu et al., 1988; Shinoda et al., 1986, 1988; Uchino et al., 1988, 1990; Uchino and Isu, 1992b). The VC neurons that send long axons as far as the lumbar segments of the spinal cord are distinctively termed vestibulo-spinal (VS) neurons in this review.
In the last two decades, we have focused on establishing a reliable technique for focal stimulation of vestibular receptors to evaluate neural connectivity. Here, we summarize the vestibular-related neuronal circuits for the vestibulo-ocular reflex, vestibulocollic reflex, and vestibulospinal reflex arcs. The focal stimulating technique also uncovered some hidden neural mechanisms. In the otolith system, we identified two hidden neural mechanisms that enhance otolith receptor sensitivity. The first is commissural inhibition, which boosts sensitivity by incorporating inputs from bilateral otolith receptors, the existence of which was in contradiction to the classical understanding of the otolith system but was observed in the utricular system. The second mechanism, cross-striolar inhibition, intensifies the sensitivity of inputs from both sides of receptive cells across the striola in a single otolith sensor. This was an entirely novel finding and is typically observed in the saccular system. We discuss the possible functional meaning of commissural and cross-striolar inhibition. Finally, our focal stimulating technique was applied to elucidate the different constructions of axonal projections from each vestibular receptor to the spinal cord. We also discuss the possible function of the unique neural connectivity observed in each vestibular receptor system.

View all citing articles on Scopus

View full text

Chapter 2 Vestibular projections to the spinal cord: the morphology of single vestibulospinal axons

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Brain Res.

Neurosci. Lett.

Brain Res.

Cervical branching of lumbar vestibulospinal axons

J. Physiol. London

The vestibulospinal tract. Effects on alpha-motoneurones in the lumbo-sacral spinal cord in the cat.

Exp. Brain Res.

Lamina VIII interneurones interposed in crossed reflex pathways in the cat

J. Physiol. London

Intrinsic neuronal organization of the vestibular nuclear complex in the cat. A Golgi study.

Ergeb. Anal. Entw. Gesch.

The vestibulospinal tract: crossed and uncrossed effects in hindlimb motoneurones in the cat

Exp. Brain Res.

Convergence in the reciprocal la inhibitory pathway of excitation from descending pathways and inhibition from motor axon collaterals

Acta Physiol. Scand.

Convergence on interneurones mediating the reciprocal la inhibition of motoneurones. III. Effects from supraspinal pathways.

Acta Physiol. Scand.

Morphology of interneurones mediating la reciprocal inhibition of motoneurones in the spinal cord of the cat

J. Physiol. London

Postsynaptic influences on the vestibular non-Deiters' nuclei from primary vestibular nerve

Exp. Brain Res.

Descending pathways with monosynaptic action on motoneurones

Experienlia

Monosynaptic excitation of alpha motoneurones from supraspinal structures in the cat

Acta Physiol. Scand.

Labyrinthine influence on cat forelimb motoneurons

Exp. Brain Res.

Arborisations dendritiques étude topo-graphique et quantitative dans le noyau vestibulaire du chat

Arch. Ital. Biol

Origin and termination of fibers from the vestibular nuclei descending in the medial longitudinal fasciculus. An experimental study with silver impregnation methods in the cat.

J. Neurol.