Collateral Actions of Premotor Interneurons on Ventral Spinocerebellar Tract Neurons in the Cat

Abstract

Jankowska E, Krutki P, Hammar I. Collateral actions of premotor interneurons on ventral spinocerebellar tract neurons in the cat. J Neurophysiol 104: 1872-1883, 2010. First published August 11, 2010 doi:10.1152/jn.00408.2010. Strong evidence that premotor interneurons provide ventral spinocerebellar tract (VSCT) neurons with feedback information on their actions on motoneurons was previously found for Ia inhibitory interneurons and Renshaw cells, while indications for similar actions of other premotor interneurons were weaker and indirect. Therefore the aim of the present study was to reexamine this possibility with respect to interneurons relaying actions of group Ib afferents from tendon organs and group II afferents from muscle spindles. In all, 133 VSCT neurons in the L3-L5 segments (including 41 spinal border neurons) were recorded from intracellularly in deeply anesthetized cats to verify that stimuli applied in motor nuclei evoked monosynaptic inhibitory postsynaptic potentials (IPSPs) attributable to stimulation of axon collaterals of premotor interneurons. IPSPs were found in over two thirds of the investigated neurons. When intraspinal stimuli were preceded by stimuli applied to a muscle nerve at critical intervals, IPSPs evoked from motor nuclei were considerably reduced, indicating a collision of nerve volleys in axons of interneurons activated by group I and group II afferents. In individual VSCT neurons monosynaptic IPSPs were evoked from both bicepssemitendinosus and gastrocnemius-soleus motor nuclei, in parallel with disynaptic IPSPs from group Ib and group II as well as group Ia afferents. These observations indicate that individual VSCT neurons may monitor the degree of inhibition of both flexor and extensor motoneurons by premotor interneurons in inhibitory pathways from group Ib and group II afferents to motoneurons. They may thus be providing the cerebellum with feedback information on actions of these premotor interneurons on motoneurons.

Rhythmic activity of feline dorsal and ventral spinocerebellar tract neurons during fictive motor actions

“…Populations of inhibitory interneurons that project to VSCT cells include reciprocal Ia inhibitory interneurons (Lindstrom and Schomburg 1974), nonreciprocal "Ib" inhibitory interneurons (Jankowska et al 2010;Lundberg and Weight 1971), and group "Ib/group II" inhibitory interneurons (Jankowska et al 2010). No disynaptic inhibitory input from reciprocal Ia inhib- itory interneurons was found in DSCT cells (Hongo et al 1983a;Lindstrom and Takata 1977), but "Ib" inhibitory interneurons (Hongo et al 1983a;1983b), as well as group Ib/II inhibitory interneurons (Jankowska and Puczynska 2008), contact DSCT cells.…”

Inhibitory inputs to four types of spinocerebellar tract neurons in the cat spinal cord

“…By using electrophysiological criteria to classify individual neurons while searching for cells to be labelled we were also able to select subpopulations of particular interest, e.g. neurons of a subpopulation of SB cells with a dominant inhibitory input from peripheral afferents and monosynaptic input from reticulospinal tract neurons (Burke et al, 1971a;Jankowska et al, 2010;Hammar et al, 2011). Furthermore, intracellular labelling provides a much more complete visualisation of the whole dendritic tree.…”

“…Postsynaptic and presynaptic inhibitory actions on various populations of spinocerebellar neurons may also vary as much as the excitatory ones, both in origin and degree (Lundberg and Weight, 1971;Burke et al, 1971a;Edgley and Jankowska, 1988;Jankowska and Puczynska, 2008;Jankowska et al, 2010;Krutki et al, 2011). The aim of the present study was therefore to extend our previous investigation of excitatory input to four types of spinocerebellar tract neurons based on immunohistochemical analysis of nerve terminals in contact with labelled neurons (Shakya- by making a similar analysis of inhibitory input to these neurons.…”

“…Electrophysiological studies revealed particularly strong inhibitory input to SB and VSCT neurons which in some cells practically constitutes the exclusive input from the periphery (Eccles et al, 1961;Oscarsson, 1965;Lundberg and Weight, 1971;Burke et al, 1971a;Hammar et al, 2011;. Inhibition of these neurons is evoked to a great extent by collateral actions of premotor interneurons, (most of which would mediate disynaptic inhibition from group Ia, Ib and II afferents), Renshaw cells and high-threshold muscle, skin and joint afferents, in parallel with their actions on motoneurons (Hultborn et al, 1971;Lundberg, 1971;Schomburg, 1973, 1974;Jankowska et al, 2010). The same interneurons would also mediate inhibition of spinocerebellar neurons from descending tract neurons (Baldissera and Roberts, 1976;Baldissera and ten Bruggencate, 1976;Hammar et al, 2011;Jankowska et al, 2011).…”

“…However, in some spinocerebellar neurons inhibition may play a more essential role because a reduction or even arrest of firing in these neurons may be a source of information for their cerebellar target cells itself (Lundberg, 1971;Hammar et al, 2011). This may apply particularly to the subpopulation of ventral spinocerebellar neurons in which peripheral input is mainly or almost exclusively inhibitory (Burke et al, 1971a;Jankowska et al, 2010;.…”