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Segmentation of the mouse fourth deep lumbrical muscle connectome reveals concentric organisation of motor units
Author(s) -
Hirst Theodore C.,
Ribchester Richard R.
Publication year - 2013
Publication title -
the journal of physiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.802
H-Index - 240
eISSN - 1469-7793
pISSN - 0022-3751
DOI - 10.1113/jphysiol.2013.258087
Subject(s) - motor unit , neuroscience , motor unit recruitment , axon , biology , motor neuron , anatomy , segmentation , motor system , connectome , computer science , artificial intelligence , spinal cord , electromyography , functional connectivity
Key points• An accelerated image segmentation algorithm was developed and applied to analysis of motor unit arborisation and connectivity (the ‘connectome’) in fourth deep lumbrical muscles (4DL) of mice expressing fluorescent proteins as morphological reporters. • Mouse 4DL muscles contain between 4 and 9 motor units and motor unit size in these muscles ranged from 3 to 111 muscle fibres. • Small motor units were restricted in their arbors to the vicinity of the nerve entry point. Larger motor units concentrically occupied muscle fibres located progressively further from the nerve entry point. • Motor unit size was weakly correlated with motor endplate size, suggesting a hierarchy of motor unit sizes based on synaptic strength. • The data suggest a segregated organisation of motor units in cylindrical muscles that has not previously been appreciated and indicate the direction of future studies required to establish possible relationships between the strengths of synaptic connections and motor unit size.Abstract Connectomic analysis of the nervous system aims to discover and establish principles that underpin normal and abnormal neural connectivity and function. Here we performed image analysis of motor unit connectivity in the fourth deep lumbrical muscle (4DL) of mice, using transgenic expression of fluorescent protein in motor neurones as a morphological reporter. We developed a method that accelerated segmentation of confocal image projections of 4DL motor units, by applying high resolution (63×, 1.4 NA objective) imaging or deconvolution only where either proved necessary, in order to resolve axon crossings that produced ambiguities in the correct assignment of axon terminals to identified motor units imaged at lower optical resolution (40×, 1.3 NA). The 4DL muscles contained between 4 and 9 motor units and motor unit sizes ranged in distribution from 3 to 111 motor nerve terminals per unit. Several structural properties of the motor units were consistent with those reported in other muscles, including suboptimal wiring length and distribution of motor unit size. Surprisingly, however, small motor units were confined to a region of the muscle near the nerve entry point, whereas their larger counterparts were progressively more widely dispersed, suggesting a previously unrecognised form of segregated motor innervation in this muscle. We also found small but significant differences in variance of motor endplate length in motor units, which correlated weakly with their motor unit size. Thus, our connectomic analysis has revealed a pattern of concentric innervation that may perhaps also exist in other, cylindrical muscles that have not previously been thought to show segregated motor unit organisation. This organisation may be the outcome of competition during postnatal development based on intrinsic neuronal differences in synaptic size or synaptic strength that generates a territorial hierarchy in motor unit size and disposition.