Elsevier

Brain Research Reviews

Volume 57, Issue 1, January 2008, Pages 46-55
Brain Research Reviews

Review
Spinal interneuronal networks in the cat: Elementary components

https://doi.org/10.1016/j.brainresrev.2007.06.022Get rights and content

Abstract

This review summarises features of networks of commissural interneurones co-ordinating muscle activity on both sides of the body as an example of feline elementary spinal interneuronal networks. The main feature of these elementary networks is that they are interconnected and incorporated into more complex networks as their building blocks. Links between networks of commissural interneurones and other networks are quite direct, with mono- and disynaptic input from the reticulospinal and vestibulospinal neurones, disynaptic from the contralateral and ipsilateral corticospinal neurones and fastigial neurones, di- or oligosynaptic from the mesencephalic locomotor region and mono-, di- or oligosynaptic from muscle afferents. The most direct links between commissural interneurones and motoneurones are likewise simple: monosynaptic and disynaptic via premotor interneurones with input from muscle afferents. By such connections, a particular elementary interneuronal network may subserve a wide range of movements, from simple reflex and postural adjustments to complex centrally initiated phasic and rhythmic movements, including voluntary movements and locomotion. Other common features of the commissural and other interneuronal networks investigated so far is that input from several sources is distributed to their constituent neurones in a semi-random fashion and that there are several possibilities of interactions between neurones both within and between various populations. Neurones of a particular elementary network are located at well-defined sites but intermixed with neurones of other networks and distributed over considerable lengths of the spinal cord, which precludes the topography to be used as their distinguishing feature.

Introduction

Elementary spinal interneuronal networks are very simple. In the simplest cases, there are just one or two interneurones in series between input neurones and motoneurones. However, even in the simplest networks, there is a number of interneurones of each kind in parallel and these neurones integrate somewhat different combinations of information, from not only their main sources of input, e.g. muscle and skin afferents, but also from other neuronal networks. They forward it also to somewhat different combinations of their target neurones, including interneurones of other neuronal networks. Because of their links with other networks, all elementary networks may thus be considered to be components of more complex networks.

This arrangement may be illustrated with any of the previously investigated networks of spinal interneurones, from Renshaw cells and interneurones mediating Ia reciprocal inhibition, which were among the first interneurones to be analysed (for references, see Jankowska, 1992), through cervical propriospinal neurones (Lundberg, 1979) and interneurones mediating reflex actions of group II muscle spindle afferents (Jankowska et al., 2002a, Jankowska et al., 2002b), to mention only those known in most detail. In this review it will be illustrated with the recently investigated networks of commissural interneurones. These networks have become of particular interest as being attributed a critical role in locomotor networks (for references, see Buchanan, 1999, Grillner, 2003, Kiehn, 2006, Soffe et al., 1984) because they are needed to adjust rhythmic activity of neurones on both sides of the spinal cord and because they are one of the major targets of reticulospinal neurones that are involved in initiation of locomotion. There is also a growing body of evidence that commissural interneurones may be of critical importance for other centrally or reflexly initiated phasic movements, including voluntary movements and postural adjustments, and that individual commissural interneurones may contribute to several of these movements.

Section snippets

Functional differentiation of the population of commissural interneurones

As other spinal interneuronal populations, the population of commissural interneurones is not homogenous. It includes subpopulations of both excitatory (glutamatergic) and inhibitory (glycinergic) neurones (Bannatyne et al., 2003, Bannatyne et al., 2006, Butt and Kiehn, 2003, Nissen et al., 2005, Roberts et al., 1988, Sugiuchi et al., 1995), at different locations (Bannatyne et al., 2003, Bannatyne et al., 2006, Harrison et al., 1986, Huang et al., 2000, Kiehn and Butt, 2003, Lu et al., 2001,

Comparison of internal organization of elementary interneuronal networks

One of the common features of the so far analysed elementary interneuronal networks is that input to each interneuronal population is drawn from a number of sources, and that input from any of these sources is distributed to several populations, although in different combinations, e.g. both Ia and Ib afferents provide input to interneurones mediating non-reciprocal inhibition of motoneurones (Jankowska et al., 1981), but Ia afferents are the main source of peripheral input to interneurones

Which neurones do and which do not belong to a neuronal network

Boundaries between different neuronal networks may be considered as not being sharp, especially when individual neurones form part of different networks under different circumstances and when neuronal networks change their configuration and elements depending on which movements they subserve. It may thus be a matter of personal preferences whether different kinds of neurones are classified as belonging to the same, or to different, networks. However, independently of how spinal interneuronal

Acknowledgments

The studies carried out in the author's laboratory were supported by grants from the NINDS/NIH (R01 NS040863) and the Swedish Research Council (15393-01A).

References (70)

  • T. Arya et al.

    Crossed reflex actions from group II muscle afferents in the lumbar spinal cord of the anaesthetized cat

    J. Physiol. (Lond.)

    (1991)
  • S. Bajwa et al.

    Crossed actions on group II-activated interneurones in the midlumbar segments of the cat spinal cord

    J. Physiol. (Lond.)

    (1992)
  • B.A. Bannatyne et al.

    Networks of inhibitory and excitatory commissural interneurons mediating crossed reticulospinal actions

    Eur. J. Neurosci.

    (2003)
  • B.A. Bannatyne et al.

    Differential projections of excitatory and inhibitory dorsal horn interneurons relaying information from group II muscle afferents in the cat spinal cord

    J. Neurosci.

    (2006)
  • A. Birinyi et al.

    Synaptic targets of commissural interneurons in the lumbar spinal cord of neonatal rats

    J. Comp. Neurol.

    (2003)
  • E. Brink et al.

    Inhibitory interactions between interneurones in reflex pathways from group Ia and group Ib afferents in the cat

    J. Physiol. (Lond.)

    (1983)
  • G.T. Bruggencate et al.

    Interaction between the vestibulospinal tract, contralateral flexor reflex afferents and 1a afferents

    Brain Res.

    (1969)
  • J.T. Buchanan

    Commissural interneurons in rhythm generation and intersegmental coupling in the lamprey spinal cord

    J. Neurophysiol.

    (1999)
  • S.J. Butt et al.

    Firing properties of identified interneuron populations in the mammalian hindlimb central pattern generator

    J. Neurosci.

    (2002)
  • A. Cabaj et al.

    Same spinal interneurons mediate reflex actions of group Ib & II afferents and crossed reticulospinal actions

    J. Neurophysiol.

    (2006)
  • S.R. Cajal
  • A.M. Degtyarenko et al.

    Modulation of oligosynaptic cutaneous and muscle afferent reflex pathways during fictive locomotion and scratching in the cat

    J. Neurophysiol.

    (1998)
  • M. Dottori et al.

    EphA4 (Sek1) receptor tyrosine kinase is required for the development of the corticospinal tract

    Proc. Natl. Acad. Sci. U. S. A.

    (1998)
  • S.A. Edgley

    Organisation of inputs to spinal interneurone populations

    J. Physiol. (Lond.)

    (2001)
  • S.A. Edgley et al.

    An interneuronal relay for group I and II muscle afferents in the midlumbar segments of the cat spinal cord

    J. Physiol. (Lond.)

    (1987)
  • S.A. Edgley et al.

    Both dorsal horn and lamina VIII interneurones contribute to crossed reflexes from group II muscle afferents

    J. Physiol. (Lond.)

    (2003)
  • S.A. Edgley et al.

    Ipsilateral actions of feline corticospinal tract neurons on limb motoneurons

    J. Neurosci.

    (2004)
  • S. Grillner

    The motor infrastructure: from ion channels to neuronal networks

    Nat. Rev., Neurosci.

    (2003)
  • I. Hammar et al.

    The actions of monoamines and distribution of noradrenergic and serotoninergic contacts on different subpopulations of commissural interneurons in the cat spinal cord

    Eur. J. Neurosci.

    (2004)
  • P.J. Harrison et al.

    Organization of input to the interneurones mediating group I non-reciprocal inhibition of motoneurones in the cat

    J. Physiol. (Lond.)

    (1985)
  • P.J. Harrison et al.

    Lamina VIII interneurones interposed in crossed reflex pathways in the cat

    J. Physiol. (Lond.)

    (1986)
  • J.E. Hoover et al.

    Retrograde labeling of lumbosacral interneurons following injections of red and green fluorescent microspheres into hindlimb motor nuclei of the cat

    Somatosens. Mot. Res.

    (1992)
  • J. Hounsgaard et al.

    Bistability of alpha-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan

    J. Physiol. (Lond.)

    (1988)
  • A. Huang et al.

    Spinal cholinergic neurons activated during locomotion: localization and electrophysiological characterization

    J. Neurophysiol.

    (2000)
  • H. Hultborn

    Convergence on interneurones in the reciprocal Ia inhibitory pathway to motoneurones

    Acta Physiol. Scand., Suppl.

    (1972)
  • Cited by (156)

    • Dynamic Functional Connectivity of Resting-State Spinal Cord fMRI Reveals Fine-Grained Intrinsic Architecture

      2020, Neuron
      Citation Excerpt :

      To date, the mechanisms at the core of spinal RS fluctuations are still speculative. Three main processes have been hypothesized (Eippert et al., 2017b; Eippert and Tracey, 2014; Kong et al., 2014): (1) RS signals could be driven by the continuous processing of inputs from the periphery (e.g., proprioception, touch, or vibration); (2) alternatively, they potentially stem from the ongoing communication between the brain and the spinal cord, through ascending (sensory) and descending (motor) signals; (3) finally, they could be generated locally from intrinsic features of spinal activity, for instance linked to coordinated movements (e.g., bilateral coordination [Jankowska, 2008; Soteropoulos et al., 2013], breathing [Sandhu et al., 2015], or central pattern generators [Guertin and Steuer, 2009]). To further shed light on these three hypotheses, we inspected the functional roles of the fine-grained iCAPs.

    View all citing articles on Scopus
    View full text