Subpopulations and functions of long C3-C5 propriospinal neurones

doi:10.1016/0006-8993(87)91402-8

Brain Research

Volume 404, Issues 1–2, 24 February 1987, Pages 395-400

https://doi.org/10.1016/0006-8993(87)91402-8 Get rights and content

Abstract

Long C₃–C₅ propriospinal neurones (PNs) are classified in 3 types depending on their pyramidal and vestibular input. Thefirst type of PNs received pyramidal excitation but lacked vestibular effects. Thesecond type of PNs was excited from the medial vestibular nucleus but not from the pyramid. Thethird type of PNs was excited from the lateral vestibular nucleus either from second order neurones or from non-second order neurones. Monosynaptic excitatory postsynaptic potentials from neck afferents and/or oligosynaptic postsynaptic potentials from forelimb afferents were found in some of the PNs of the second and third type but not in those of the first type. Collision experiments revealed that cortico- and rubrospinal fibres to the long C₃–C₅ PNs terminate in the rostral spinal cord, presumably in the forelimb segments. Vestibular and reticular effects on the PNss are partly from fibres terminating in the rostral spinal cord and partly from fibres projecting to the lumbar cord. It is postulated that the different types of PNs contribute to the adjustment of hindlimb posture which is required during different movements of the forebody. It is suggested that the basic tonus is maintained mainly by the direct projection to the hindlimb segments from lateral vestibulospinal and reticulospinal neurones which excite antigravity muscles via lumbar interneurones and that long C₃-C₅ PNs converge onto the same interneurones so that they act by modulation of the bsic tonus.

Reference (31)

AlstermarkB. et al.
Long C₃-C₅ propriospinal neurones in the cat
Brain Research
(1987)
JankowskaE. et al.
Propriospinal control of last order interneurones of spinal reflex pathways in the cat
Brain Research
(1973)
KeninsP. et al.
Short- and long-latency reflex pathways from neck afferents to hindlimb motoneurones in the cat
Brain Research
(1978)
LundbergA.
Multisensory control of spinal reflex pathways
SchomburgE.D. et al.
Functional organization of the spinal reflex pathways from forelimb afferents to hindlimb afferents to hindlimb motoneurones in the cat
Brain Research
(1978)
SkinnerR.D. et al.
Responses of long descending propriospinal neurons to natural and electrical types of stimuli in cat
Brain Research
(1980)
SkinnerR.D. et al.
Monosynaptic activation of long descending propriospinal neurons from the lateral vestibular nucleus and the medial longitudinal fasciculus
Exp. Neurol.
(1984)
AbzugC. et al.
Cervical branching of lumbar vestibular axons
J. Physiol. (London)
(1974)
...
AlstemarkB. et al.
Vestibular effects in long C₃-C₅ propriospinal neurones
Brain Research
(1987)

AlstermmarkB. et al.

Integration in the descending pathways controlling the forelimb afferents to C₃-C₅ propriospinal neurones

Exp. Brain Res.

(1984)

AlstermarkB. et al.

Timing of postural adjustment in relation to forelimb target-reaching in cats

Acta Physiol. Scand.

(1985)

BaldisseraF. et al.

Effects of the vestibulospinal tract on transmission from primary afferents to ventral spino-cerebellar tract neurones

Acta. Physiol. Scand.

(1976)

BoyleR. et al.

convergence and interaction of neck and muscular vestibular inputs on vestibulospinal neurons

J. Neurophysiol.

(1981)

...

Cited by (64)

Long-Distance Descending Spinal Neurons Ensure Quadrupedal Locomotor Stability
2016, Neuron
Citation Excerpt :
Together, our findings reveal that cervical and lumbar spinal segments are bidirectionally coupled by distinct neuronal subpopulations identified by NT identity and projection laterality. We focused our subsequent analyses mostly on the elucidation of identity and function of cervico-lumbar projection neurons, due to their predicted involvement in transmitting supraspinal commands to lumbar circuits (Alstermark et al., 1987b; Mitchell et al., 2016). To map the precise location of cervico-lumbar projection neurons and their cellular identity, we carried out retrograde tracing experiments from the lumbar spinal cord.
Locomotion is an essential animal behavior used for translocation. The spinal cord acts as key executing center, but how it coordinates many body parts located across distance remains poorly understood. Here we employed mouse genetic and viral approaches to reveal organizational principles of long-projecting spinal circuits and their role in quadrupedal locomotion. Using neurotransmitter identity, developmental origin, and projection patterns as criteria, we uncover that spinal segments controlling forelimbs and hindlimbs are bidirectionally connected by symmetrically organized direct synaptic pathways that encompass multiple genetically tractable neuronal subpopulations. We demonstrate that selective ablation of descending spinal neurons linking cervical to lumbar segments impairs coherent locomotion, by reducing postural stability and speed during exploratory locomotion, as well as perturbing interlimb coordination during reinforced high-speed stepping. Together, our results implicate a highly organized long-distance projection system of spinal origin in the control of postural body stabilization and reliability during quadrupedal locomotion.
Schwann cell transplantation and descending propriospinal regeneration after spinal cord injury
2015, Brain Research
Citation Excerpt :
The laPST system was found to play an important role in locomotion by coupling neural activity in cervical and lumbar enlargements (Cote et al., 2012; Miller et al., 1973). Propriospinal neurons receive strong and convergent supraspinal innervations including those from the corticospinal (CST), rubrospinal (RST), reticulospinal (ReST) and vestibulospinal (VST) tracts (Alstermark et al., 1987, 1991b; Illert et al., 1977; Kostyuk and Vasilenko, 1978; Nishimura et al., 2009; Robbins et al., 1992; Skinner et al., 1979). Such signal relay has significance in transporting supraspinal command down to the spinal cord not only in normal physiological but also in pathological conditions (Fig. 1).
After spinal cord injury (SCI), poor ability of damaged axons of the central nervous system (CNS) to regenerate causes very limited functional recovery. Schwann cells (SCs) have been widely explored as promising donors for transplantation to promote axonal regeneration in the CNS including the spinal cord. Compared with other CNS axonal pathways, injured propriospinal tracts display the strongest regenerative response to SC transplantation. Even without providing additional neurotrophic factors, propriospinal axons can grow into the SC environment which is rarely seen in supraspinal tracts. Propriospinal tract has been found to respond to several important neurotrophic factors secreted by SCs. Therefore, the SC is considered to be one of the most promising candidates for cell-based therapies for SCI. Since many reviews have already appeared on topics of SC transplantation in SCI repair, this review will focus particularly on the rationale of SC transplantation in mediating descending propriospinal axonal regeneration as well as optimizing such regeneration by using different combinatorial strategies.
This article is part of a Special Issue entitled SI: Spinal cord injury.
Ascending and descending propriospinal pathways between lumbar and cervical segments in the rat: Evidence for a substantial ascending excitatory pathway
2013, Neuroscience
Citation Excerpt :
The principal findings of the present study are summarised in Fig. 11. The most complete electrophysiological studies of long-descending PSNs were performed by Alstermark et al. (1987a,b,c) who studied PSNs in the C3–C5 segments of cats. These cells have highly convergent inputs from a variety of motor control systems; some have convergent input from the lateral and medial vestibulospinal tracts along with neck and forelimb proprioceptors whereas others have input principally from the corticospinal tract.
Precise mechanisms are required to coordinate the locomotor activity of fore- and hind-limbs in quadrupeds and similar mechanisms persist to coordinate movement of arms and legs in humans. Propriospinal neurons (PSNs) are major components of the networks that coordinate these mechanisms. The b subunit of cholera toxin (CTb) was injected unilaterally into either L1 or L3 segments in order to label ascending and descending propriospinal pathways. Labelled cells were examined with light or confocal microscopy. Cells projecting to lumbar segments were evenly distributed, bilaterally throughout all cervical segments. However many more cells were labelled from L1 injections than L3 injections. Roughly 15% of cells in both sides of the C2 segment was found to be immunoreactive for calretinin and a small number (4%) was immunoreactive for calbindin. Axons projecting from L1 to cervical segments formed predominant ipsilateral projections to the cervical intermediate grey matter and ventral horn. Very large numbers of terminals were concentrated within the ventrolateral motor (VLM) nuclei of C7–8 segments but there was sparse innervation of the contralateral nucleus. The vast majority (85%) of these axon terminals in the ipsilateral VML was immunoreactive for the vesicular glutamate transporter 2 (VGLUT2) and the remaining 15% was immunoreactive for the vesicular GABA transporter (VGAT); many of these contained GABA and/or glycine. Inhibitory and excitatory terminals were also found in the contralateral VLM. Most of the terminals in the VLM made contacts with motoneurons. The major finding of this study is the existence of a substantial excitatory propriospinal pathway that projects specifically to the VLM. Motoneurons in the VLM supply muscles of the axilla therefore this pathway is likely to have a profound influence on the activity of the shoulder joint. This pathway may synchronise lumbar and cervical pattern generators and hence the coordination of locomotor activity in the fore- and hind limbs.
Neural coupling between the upper and lower limbs in humans
2007, Neuroscience Letters
The aim of this study was to establish the effects of active sinusoidal ipsilateral and contralateral upper limb flexion, extension, abduction, and adduction with elbows extended on the right soleus H-reflex with subjects seated and standing. Reflex effects were also established when both arms moved synchronously in a reciprocal pattern with elbows flexed in seated and standing subjects. Sinusoidal arm movements were timed to a metronome and performed at 0.2 Hz. Soleus H-reflexes were elicited only once (every 4 s) in every movement cycle of the upper limbs. Position of arms, and activity of shoulder muscles were recorded through twin-axis goniometers and surface electromyography (EMG), respectively. We found that in seated subjects, regardless the direction of the active movement or the upper limb being moved, the soleus H-reflex was depressed. In standing subjects, a reflex depression was observed during extension, abduction, and adduction of the ipsilateral and contralateral upper limbs. Muscles were active during arm flexion and abduction in all directions of arm movement with subjects either seated or standing. It is suggested that arm movement might be incorporated in the rehabilitation training of people with a supraspinal or spinal cord lesion, since it can benefit motor recovery by decreasing spinal reflex excitability of the legs in these patients.
Moving toward elucidating alternative motor pathway structures post-stroke: the value of spinal cord neuroimaging
2024, Frontiers in Neurology
Spinal Interneurons: Diversity and Connectivity in Motor Control
2023, Annual Review of Neuroscience

View all citing articles on Scopus

^*: Present address: Department of Anatomy, Medical College of Pennsylvania at EPPI, 3200 Henry Avenue, Philadelphia, PA 19129, U.S.A.

^**: Department of Neurophysiology, Institute of Brain Research, School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113, Japan

View full text

Subpopulations and functions of long C3-C5 propriospinal neurones

Abstract

Brain Research

Brain Research

Brain Research

Brain Research

Brain Research

Exp. Neurol.

Cervical branching of lumbar vestibular axons

J. Physiol. (London)

Vestibular effects in long C3-C5 propriospinal neurones

Brain Research

Integration in the descending pathways controlling the forelimb afferents to C3-C5 propriospinal neurones

Exp. Brain Res.

Timing of postural adjustment in relation to forelimb target-reaching in cats

Acta Physiol. Scand.

Effects of the vestibulospinal tract on transmission from primary afferents to ventral spino-cerebellar tract neurones

Acta. Physiol. Scand.

convergence and interaction of neck and muscular vestibular inputs on vestibulospinal neurons

J. Neurophysiol.

Subpopulations and functions of long C₃-C₅ propriospinal neurones

Vestibular effects in long C₃-C₅ propriospinal neurones

Integration in the descending pathways controlling the forelimb afferents to C₃-C₅ propriospinal neurones