Muscle Spindles in Extraocular Muscles of Human Infants

Abstract

The capacity of muscle spindles in adult human extraocular muscles (EOM) to provide effective proprioception was questioned on the grounds of their peculiar morphology. Their appearance could be attributable to ageing and to test this possibility examples of infant muscle spindles have been examined. Forty encapsulated structures from five extraocular muscles removed post mortem from 4 infant patients aged 6 days, 5, 23 and 30 months were examined by means of light microscopy using serial transverse sections. Seven of them were identified as false spindles. The remaining 33 structures, identified as spindles, contained a total of 175 intrafusal fibres varying from 2 to 12 (mean: 6) in each. 130 of these fibres (74.3%) were of nuclear chain type. Unequivocal evidence of bag fibres was not found. Spindles lacked or had a limited equatorial expansion, and the inner capsule was incomplete and irregularly shaped. 45 (25.7%) of the intrafusal fibres had extrafusal features with large diameters, peripherally placed nuclei, no equatorial modification and without associated sensory nerve terminals. Serial sections revealed that a majority of the nuclear chain fibres were interrupted, fragmented or terminated abruptly, and most spindles contained at least one incomplete fibre. These observations show that the atypical features observed in adult human EOM spindles are also present in infants and are therefore not attributable to ageing.

How does the structure of extraocular muscles and their nerves affect their function?

“…1,[35][36][37] They also differ from spindles in EOMs of other mammals. 3 Their numbers may have been overestimated in previous studies because encapsulated spindle-like structures, with unmodified intrafusal fibres lacking sensory neuronal contacts, are also present in human EOMs.…”

“…3 Their numbers may have been overestimated in previous studies because encapsulated spindle-like structures, with unmodified intrafusal fibres lacking sensory neuronal contacts, are also present in human EOMs. [37][38][39] These anomalous fibres found in so-called false spindles, are also observed in true spindles. Bruenech and Ruskell 37 reported that 25.7% of the intrafusal fibres in 40 spindles were anomalous, lacking equatorial modifications and sensory endings, some of which were found embedded into the capsule wall ( Figure 6).…”

“…These and other noted peculiarities, which have not been observed in muscle spindles in the EOMs of other species, 3 give reason to question the spindles' proprioceptive capacity in man. 37 However, studies based on myosin heavy chain investigations have reached alternative conclusions and promote the view that the anomalous fibres might reflect dynamic structures that support modulating and adapting processes in advancing age and throughout life. 35 This hypothesis is attractive in view of the labile neuromuscular organisation and numerous age-related changes that have been observed in human EOMs (described below).…”

The Oculomotor Systems Ability to Adapt to Structural Changes Caused by the Process of Senescence: A Review

“…Proprioceptors, such as muscle spindles and tendon receptors, are present in human extraocular muscles. Although their structural organisation departs from their somatic counterparts (Bruenech & Ruskell, 2001;Ruskell, 1999), they are argued to have some capacity to monitor muscle length and force (Lennerstrand, 2007;Park, Sa, & Oh, 2009). Efference copy, on the other hand, is based on the notion that the brain uses a copy of the efferent signal to the extraocular muscles to calculate eye position (Wurtz, 2008).…”

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“…Recent publications have argued that some of the neural elements may represent motor endplates (Blumer et al, 2001), yet some uncertainty remains. Muscle spindles are also present in the extraocular muscles, but due to certain peculiar features their proprioceptive capacity has been questioned (Bruenech and Ruskell, 2001). Again, some uncertainty remains.…”