Mammalian facial muscles contain muscle spindles

Abstract

Muscle spindles are sensory receptors in skeletal muscle that provide information on muscle length and velocity of contraction. Previous studies noted that facial muscles lack muscle spindles, but recent reports indicate that the human platysma muscle and “buccal” muscles contain spindles. Mammalian facial muscles are active in social communication, vibrissa movement, and vocalizations, including human speech. Given these functions, we hypothesized that facial muscles contain muscle spindles, and we predicted that humans would have the greatest number, given the role our lips play in speech. We examined previously sectioned and stained (with H&E and trichrome stains) orbicularis oris (upper fibers) and zygomaticus (major) muscles across a broad phylogenetic range of mammalian species, spanning a wide distribution of body size and ecological niche, to assess the presence of muscle spindles. We also stained several sections with Sirius red to highlight the muscle spindle capsule. Our results indicate that mammalian facial muscles contain muscle spindles, supporting our hypothesis. Contrary to our prediction, though, humans (and other primates) had the lowest number of muscle spindles. We instead found that the carnivoran sample and the horse sample had the greatest number of spindles. Larger body size and nocturnality were also associated with a greater number of spindles. These results must be viewed with caution, though, as our sample size was small and there are critical mammalian taxa missing. Future work should use an expanded phylogenetic range of mammalian species to ascertain the role that phylogeny plays in muscle spindle presence and count.

Proprioceptive innervation of the human lips

“…Therefore, a putative facial proprioceptive system, if present, must be represented by other structures not yet identified. Nevertheless, muscle spindles are present muscles innervated by the facial nerve like m. platysma colli muscle (May et al, 2018(May et al, , 2022, and recently, Omstead et al (2023) hypothesized that facial muscles contain muscle spindles, and predicted that humans would have the greatest number, given the role our lips play in speech. We have repeatedly investigated the occurrence of muscle spindles in human cephalic muscles, and we have never found muscle spindles in facial muscles (see for a review Cobo et al, 2019;Cobo, Junquera, et al, 2021;Cobo, García-Piqueras, et al, 2021).…”

“…Despite this, muscle spindles are present in muscles innervated by the facial nerve like m. platysma colli (May et al, 2018(May et al, , 2022. Recently, Omstead et al (2023) hypothesized that facial muscles contain muscle spindles and predicted that humans would have the greatest number compared to other species, given the role our lips play in speech. But these authors found a very low density of muscle spindles in human facial muscles and failed to demonstrate support for their hypothesis.…”

“Untying the knot”: The primitive orofacial muscle architecture in the gorilla (Gorilla gorilla) as a key to the evolution of hominin facial movement

“…They have also been linked to the unique human ability of speech. [11][12][13][14][15] Facial expressions are phylogenetically shared across many non-human primates. Accordingly, studying facial expression in these species is essential to understanding the evolution of facial expression in modern humans.…”

“…In this regard, studying the facial anatomy of Pan troglodytes (henceforth, chimpanzee) was of particular importance, since the chimpanzee is our closest living relative. While a number of studies have addressed the chimpanzee facial anatomy, 3,13,15,[44][45][46] information on the facial anatomy of humans' second closest living relative, Gorilla gorilla (henceforth, gorilla), is insufficient as it relies on limited investigations. 27,31,47 Since chimpanzees are closer to humans than they are to gorillas, 48 and since it has been suggested that the arrangement and complexity of facial muscles in the chimpanzee are more similar to that in Homo sapiens than was previously claimed, 37 information on the facial anatomy of the gorilla would be instructive.…”

“…In the primate order, human faces are exceptionally mobile and have unique anatomical features that have been linked to their communication faculties, e.g., white sclera and deeply shaded red lips (vermilion). They have also been linked to the unique human ability of speech 11–15 …”