Spinal interneuronal networks in the cat: elementary components

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.

Figure 1. Axonal projections of commissural interneurones

A, an example of exclusively contralateral projections of lamina VIII neurobiotin labelled interneurones with input from reticulospinal neurones in adult cat, with the trajectory of the main axonal branches, as indicated, and terminal projection areas shaded (Modified from Fig. 9 in Bannatyne et al., 2003). B. summary of axonal branching of intraaxonally labelled adult laminae VIII interneurones with input from reticulospinal neurones; all collaterals given of contralaterally (to the left of the dashed lines indicating the midline (Modified from Fig. 6 in Matsuyama et al., 2004). C and D, bilateral projections of inhibitory dorsal horn interneurones with input from group II afferents but only ipsilateral of excitatory ones (Modified from Fig. 7 & 8 in Bannatyne et al., 2006). Shaded areas in C and D indicate the total terminal projected areas of the reconstructed axonal branches. E and F. bilateral projections of lamina VIII commissural interneurones in a newborn kitten and mouse (Golgi staining; modified from Fig. 5 and 8 in Scheibel and Scheibel, 1966).

Figure 2. Incorporation of commissural interneurones with monosynaptic input from reticulospinal neurones into other spinal networks

The grey circle represents commissural interneurones targeting contralateral motoneurones. Other circles represent commissural interneurones (Co C) on the opposite side of the spinal grey matter, reticulospinal (RS) neurones with axons in the ipsilateral medial longitudinal fascicle (MLF), neurones in the lateral Vestibular nucleus (LVN), ipsilateral and contralateral pyramidal tract (PT) neurones, and neurones in the ipsilateral mesencephalic locomotor region (MLR) and cerebellar fastigial nucleus (FN). Records A–D and G–I, are from commissural interneurones which were antidromically activated from the contralateral GS motor nuclei, while those in E are from a GS motoneurone and in F from an unspecified commissural neurone. They show PSPs (or action potentials in F) evoked by stimulation of the indicated structures. Dotted lines in A–E indicate: stimulus artefacts, descending volleys following the MLF or VS stimuli, onset of monosynaptic EPSPs and onset of di- or trisynaptically evoked EPSPs. Dotted lines in G–I indicate afferent volleys from the Q nerve and onset of disynaptic EPSPs and IPSPs evoked by them. The records are: A–C from Fig. 6 in Jankowska et al.(2006); D from Fig. 1 in Krutki et al. (2003); E from Fig. 5 in Matsuyama and Jankowska (2004); F from Fig. 8 in Matsuyama et al.(2004); G–I from Figs. 5 & 7 in Jankowska et al. (2005).

Figure 3. Enhancement of synaptic actions in the double crossed pathways between ipsilateral PT neurones and motoneurones

A and B, enhancement of EPSPs evoked by pyramidal tract (PT) and medial longitudinal fascicle (MLF) stimuli in a GS motoneurone after systemic application of the K⁺ channel blocker 4-aminopyridine (4-AP) Modified from Fig. 2 in Jankowska et al.(2005). C. diagram of connections in these pathways, via reticulospinal (RS) neurones and lamina VIII commissural interneurones and sites of recording from a motoneurone (MN) in A and B and of recording from interneurones and of ionophoresis in D and E. D and E. Histograms of mean numbers of spike potentials evoked in commissural interneurones by 20 stimuli applied within the MLF before (light grey; control & placement), during (dark grey) and after (light grey; recovery) ionophoresis of noradrenaline (NA) and serotonin (5-HT) Modified from Fig. 4 in Hammar et al. (2004)

Figure 4. Terminal projection areas of lamina VIII commissural interneurones with input from RS neurones outside motor nuclei

A and D, records from two excitatory interneurones with monosynaptic EPSPs from the MLF (<1 ms latency from the descending volleys indicated by the first dotted lines). Both were antidromically activated from the gastrocnemius-soleus GS) motor nuclei, but only the first was found to project to motor nuclei in the L5 segment (B) and their projections outside motor nuclei differed. In the L5 segment (B) they were in the ventral horn dorsal and medial to motor nuclei (upper box) and in the L4 segment (E) in the more dorsal part of lamina VII. In both areas a considerable number of terminal were found (C and F). Modified from Fig. 7 and 9 in Bannatyne et al. (2003). Diagram shows hypothetical target cells (light grey) of lamina VIII commissural interneurones (dark grey) outside motor nuclei; dotted line indicates midline.

Figure 5. Examples of disynaptic PSPs evoked from the MLF via commissural interneurones - at the same latency in motoneurones and in interneurones in pathways from group Ib and II afferents and thus indicating collateral actions of commissural interneurones on other premotor interneurones

A–F, Intracellular records (upper traces) from four interneurones with input from group Ib afferents (illustrated in C) or group II afferents (illustrated in F) in which disynaptic EPSPs (left panels) or IPSPs (middle panels) were evoked from the MLF. As judged by antidromic activation from motor nuclei such interneurones were premotor interneurones in pathways from group Ib or II afferents. G–H, Records from two GS motoneurones aligned with respect to MLF volleys evoked by the 3^rd stimulus; the volleys are indicated by the first dotted lines and the onset of the PSPs by the second. I, Diagram showing collateral connections between MLF and the two kinds of interneurones illustrated in A–F. The circles represent subpopulations of interneurones of the various populations but the indicated connections apply to individual interneurones of these subpopulations. J–L, Evidence that disynaptic Ib IPSPs evoked in motoneurones (K) are mediated by interneurones co-excited from the MLF because they are facilitated (L) when preceded by MLF stimuli. Note much greater amplitude of IPSPs evoked when stimulation of Ib afferents was preceded by stimulation of the MLF (black traces in L) than when it was not (K and grey traces in L). Such records substantiate connections indicated in I and postulated on the basis of the data illustrated in Fig. 4. Modified from Figs 3, 4 and 8 in Cabaj et al. (2006).

Figure 6. Depression of IPSPs evoked in motoneurones from the MLF, LVN and PT by Renshaw cells activated by stimulation of motor axons as the evidence that the IPSPs are mediate by Ia inhibitory interneurones

Top row, test IPSPs alone. Middle row IPSPs evoked by the same stimuli but after conditioning stimulation of a muscle nerve followed by activation of Renshaw cells. Bottom row, superposition of the test (black) and conditioned (grey, smaller) IPSPs. All the records are averages of 20 single records. Left diagram, pathways via which IPSPs illustrated in A–D were evoked. These from reticulospinal (RS) neurones with axons in the medial longitudinal fascicle (MLF) excited by pyramidal tract (PT) neurones or from vestibulospinal (VS) neurones via lamina VIII commissural interneuronesand Ia inhibitory interneurones, the latter two represented by the grey circles labelled VIII and Ia, to alpha motoneurones. Right diagram, network of Ia inhibitory interneurones (Ia) and Renshaw cells (R) with which the networks to the left were linked. A and B, modified from Fig. 2 in Jankowska et al. (2005)