Properties of axon terminals contacting intermediate zone excitatory and inhibitory premotor interneurons with monosynaptic input from group I and II muscle afferents

• Published in: The Journal of physiology Vol. 588; no. 21; pp. 4217 - 4233
• Main Authors: Liu, Ting Ting, Bannatyne, B. Anne, Jankowska, Elzbieta, Maxwell, David J.
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Publishing Ltd 01.11.2010; Wiley Subscription Services, Inc; Blackwell Science Inc
• Subjects: Afferent; Animal; Animals; Cats; Cell Communication; Cell Communication - physiology; Fysiologi; Inhibitory Postsynaptic Potentials; Inhibitory Postsynaptic Potentials - physiology; innervation; Interneurons; Interneurons - physiology; Models, Animal; Muscle; Muscle, Skeletal - innervation; Neurons; Neurons, Afferent - physiology; Neuroscience; Physiology; Presynaptic Terminals; Presynaptic Terminals - physiology; Skeletal; Synapses; Synapses - physiology; Vesicular Glutamate Transport Protein 1; Vesicular Glutamate Transport Protein 1 - physiology; Vesicular Glutamate Transport Protein 2; Vesicular Glutamate Transport Protein 2 - physiology
• ISSN: 0022-3751; 1469-7793; 1469-7793
• DOI: 10.1113/jphysiol.2010.192211

The intermediate zone of the spinal grey matter contains premotor interneurons mediating reflex actions of group I and II muscle afferents. However, limited information is available on how activity of inhibitory versus excitatory interneurons in this population are modulated and how they contribute to motor networks. There were three aims of this study: (1) to characterize excitatory axonal contacts on interneurons; (2) to determine if contact patterns on excitatory and inhibitory interneurons are different; (3) to determine if there are differences in presynaptic inhibitory control of excitatory and inhibitory interneurons. We used intracellular labelling of electrophysiologically identified cells along with immunochemistry to characterise contacts formed by axons that contain vesicular glutamate transporters (VGLUT1 and VGLUT2) and contacts formed by VGLUT1 terminals which in turn were contacted by GABAergic terminals on cells that were characterised according to their transmitter phenotype. All 17 cells investigated were associated with numerous VGLUT1 contacts originating from primary afferents, and similar contact densities were found on excitatory and inhibitory cells, but VGLUT2‐immunoreactive terminals originating from intraspinal neurons were less frequent, or were practically absent, especially on excitatory cells. Similar numbers of VGLUT1 contacts with associated GABAergic terminals were found on excitatory and inhibitory cells indicating a similar extent of presynaptic GABAergic control. However, scarce VGLUT2 terminals on intermediate zone excitatory premotor interneurons with input from muscle afferents suggest that they are not significantly excited by other spinal neurons but are under direct excitatory control of supraspinal neurons and, principally inhibitory, control of spinal neurons. The spinal cord contains networks of neurons that coordinate various types of movement by controlling muscle contraction. We investigated properties of axon terminals that supply input to a particular class of interneuron that directly excites or inhibits motoneurons that supply muscles. Analysis of the types of terminals on excitatory interneurons indicates that they are activated by sensory fibres and supraspinal neurons and that other spinal interneurons have inhibitory but not excitatory actions on them. In contrast, inhibitory interneurons are both excited and inhibited by other spinal interneurons. These findings provide us with new information about the organisation of neurons that coordinate movements and will form a basis to develop new circuit models.