Nonuniform distribution of contacts from noradrenergic and serotonergic boutons on the dendrites of cat splenius motoneurons

• Published in: Journal of comparative neurology (1911) Vol. 521; no. 3; pp. 638 - 656
• Main Authors: Montague, Steven J., Fenrich, Keith K., Mayer-Macaulay, Colin, Maratta, Robert, Neuber-Hess, Monica S., Rose, P. Ken
• Format: Journal Article
• Language: English
• Published: Hoboken Wiley Subscription Services, Inc., A Wiley Company 15.02.2013; Wiley Subscription Services, Inc
• Subjects: Adrenergic Neurons - ultrastructure; Animals; Cats; Cell Shape; Cell Size; compartmental; Dendrites - ultrastructure; dendritic tree; Female; input-output properties; monoamines; Motor Neurons - ultrastructure; Neck Muscles - innervation; neuromodulation; Norepinephrine - physiology; Presynaptic Terminals - ultrastructure; Serotonergic Neurons - ultrastructure; Serotonin - physiology; spinal cord; Spinal Cord - cytology; Studies
• ISSN: 0021-9967; 1096-9861
• DOI: 10.1002/cne.23196

The input‐output properties of motoneurons are dynamically regulated. This regulation depends, in part, on the relative location of excitatory and inhibitory synapses, voltage‐dependent and ‐independent channels, and neuromodulatory synapses on the dendritic tree. The goal of the present study was to quantify the number and distribution of synapses from two powerful neuromodulatory systems that originate from noradrenergic (NA) and serotonergic (5‐HT) neurons. Here we show that the dendritic trees of motoneurons innervating a dorsal neck extensor muscle, splenius, in the adult cat are densely, but not uniformly innervated by both NA and 5‐HT boutons. Identified splenius motoneurons were intracellularly stained with Neurobiotin. Using 3D reconstruction techniques we mapped the distributions of contacts formed by NA and 5‐HT boutons on the reconstructed dendritic trees of these motoneurons. Splenius motoneurons received an average of 1,230 NA contacts (range = 647–1,507) and 1,582 5‐HT contacts (range = 1,234–2,143). The densities of these contacts were 10 (NA) to 6 (5‐HT)‐fold higher on small compared to large‐diameter dendrites. This relationship largely accounts for the bias of NA and 5‐HT contacts on distal dendrites and is partially responsible for the higher density of NA contacts on dendrites located more than 200 μm dorsal to the soma. These results suggest that the neuromodulatory actions of NA and 5‐HT are compartmentalized and regulate the input‐output properties of motoneurons according to precisely arranged interactions with voltage‐dependent and ‐independent channels that are primarily located on small‐diameter dendrites. J. Comp. Neurol. 521:638–656, 2013. © 2012 Wiley Periodicals, Inc. Diffuse, yes; random, no. This phrase summarizes the organization of serotonergic (5‐HT) and noradrenergic (NA) synapses in motoneuron nuclei. At the level of different motoneuron pools, these synapses are distributed with little or no order. However, at the level of the dendrites of individual motoneurons, this diffuse organization is transformed into precisely arranged domains. These domains may provide the basis for highly ordered interactions between 5‐HT or NA synapses and specific combinations of excitatory and inhibitory synapses and voltage‐dependent channels.