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- MATERIALS AND METHODS
- LITERATURE CITED
Facial expression is a universal means of visual communication in humans and many other primates. Humans have the most complex facial display repertoire among primates; however, gross morphological studies have not found greater complexity in human mimetic musculature. This study examines the microanatomical aspects of mimetic musculature to test the hypotheses related to human mimetic musculature physiology, function, and evolutionary morphology. Samples from the orbicularis oris muscle (OOM) and the zygomaticus major (ZM) muscle in laboratory mice (N = 3), rhesus macaques (N = 3), and humans (N = 3) were collected. Fiber type proportions (slow-twitch and fast-twitch), fiber cross-sectional area, diameter, and length were calculated, and means were statistically compared among groups. Results showed that macaques had the greatest percentage of fast fibers in both muscles (followed by humans) and that humans had the greatest percentage of slow fibers in both muscles. Macaques and humans typically did not differ from one another in morphometrics except for fiber length where humans had longer fibers. Although sample sizes are low, results from this study may indicate that the rhesus macaque OOM and ZM muscle are specialized primarily to assist with maintenance of the rigid dominance hierarchy via rapid facial displays of submission and aggression, whereas human musculature may have evolved not only under pressure to work in facial expressions but also in development of speech. Anat Rec, 297:1250–1261, 2014. © 2014 Wiley Periodicals, Inc.
- Top of page
- MATERIALS AND METHODS
- LITERATURE CITED
The human face has long been regarded as unique relative to the faces of all other mammals, even among other members of the order Primates (Darwin, 1872; Huber, 1931; Schmidt and Cohn, 2001; Burrows, 2008; Burrows and Cohn, in press). Within humans, face recognition is associated with an assortment of cognitive and neural specializations, suggesting that it has played an important role in our evolution (van Hooff, 1962, 1972; Parr and de Waal, 1999; Parr et al., 2000; Sherwood et al., 2005; Taubert, 2010; Dobson and Sherwood, 2011a,b; Parr, 2011). The human face is the primary mechanism of our social interactions and person identification (Ekman, 1973; Ekman and Keltner, 1997; Schmidt and Cohn, 2001; Burrows and Cohn, in press) and is itself a visible signal of social intentions, motivations, and kin/individual identity (Schmidt and Cohn, 2001; Burrows, 2008). Clearly, the structural integrity of the human face is a hallmark of our species, and we depend on it for normal social interactions and a normal human lifestyle.
Facial expressions and movements are controlled by facial expression (mimetic) musculature. Mimetic muscles are branchiomeric in nature, being derived from the second (or hyoid) branchial arch, and are, as such, innervated by the seventh (facial) cranial nerve (Young, 1957; Sperber, 2001). This musculature is both morphologically and physiologically unique when compared with the striated musculature of the limbs and trunk (Standring, 2008). Unlike other striated muscles that typically attach to bony landmarks, mimetic musculature attaches into the dermis of the face, neck, and external ears. When the musculature contracts, it deforms the facial mask, producing actions associated with facial expression of emotion or intent as well as functions related to nutrient intake and vocalizations/speech. Human mimetic musculature is dominated by Type II (fast-twitch) fibers to a much higher percentage than the fast/slow distribution found in limb and trunk musculature (Schwarting et al., 1982; Stål, 1987, 1990; Happak et al., 1988; Freilinger et al., 1990; Cheng et al., 2007). This unique physiological attribute may assist in the production of spontaneous facial expressions comprising quick muscle contractions that last only a few seconds (Ekman and Friesen, 1982; Schmidt et al., 2003).
Numerous recent studies have shown that the gross anatomical aspects of human facial expression musculature, including number of muscles and attachments, are not so derived when compared with other primates (Burrows and Smith, 2003; Burrows et al., 2006, 2009, 2011; Burrows, 2008; Diogo and Wood, 2012). Yet, humans clearly have a uniquely wide range of graded, salient facial expressions and have a greater expertise at facial processing than any other primate investigated to date (van Hooff, 1962; Dobson, 2009; Parr et al., 2010; Parr, 2011; Waller et al., 2012; Caeiro et al., 2013). At the microanatomical level, previous comparative and functional studies of the orbicularis oris muscle (OOM) in humans, chimpanzees, and gibbons showed that the arrangement of muscle fibers and muscle fiber morphometrics are reflective of the evolutionary divergence of lip function among these taxa (Rogers et al., 2009; Burrows et al., 2011). Similarly, Burrows and Smith (2003) demonstrated that muscles of the external ear in galagos are microanatomically arranged more tightly with less connective tissue than musculature associated with other regions of the face. Galagos are noted in part for their discrete and complex external ear movements (e.g., Charles-Dominique, 1977). Unmistakably, aspects of mimetic musculature including muscle fiber type, fiber cross-sectional area, diameter, and length could assist our efforts at conceptualizing the functional and evolutionary differences between human facial expression musculature and that of other primates.
The contractile properties of any skeletal muscle depend largely on the proportion of slow-twitch to fast-twitch fibers. Generally, slow-twitch (Type I) fibers are slow to generate a contraction but have a high level of endurance and fatigue slowly. Fast-twitch (Type II) fibers quickly generate a contraction but have a low level of endurance and resist fatigue poorly. The ability of a muscle to do work is reflected in part by the cross-sectional area, fiber diameter, and length of the muscle fibers (Bodine et al., 1982; Gans, 1982; Lieber and Fridén, 2000; Eng et al., 2008). The length of a muscle fiber can be increased by adding sarcomeres so that a longer fiber can contract at a higher velocity (Lieber, 2002; Lieber and Fridén, 2000). Therefore, fiber length can inform our understanding of the potential speed at which a muscle can contract. Muscles that undergo repeated increased use can experience hypertrophy, and this can be accomplished by increasing the size and amount of contractile proteins within the myofibrils. This increases muscle fiber diameter and cross-sectional area, which can themselves inform our understanding of the potential contraction force that a muscle can produce (Lieber and Fridén, 2000; Paul and Rosenthal, 2002).
The relationship between muscle function and fiber type distribution is well known in mammals, and most of our understanding of this relationship comes from studies of limb and paravertebral musculature. Mammals that move quickly and engage in terrestrial quadrupedal postures tend to have limb and spinal musculature dominated by Type II (fast-twitch) fibers, whereas mammals that move slowly and engage in suspensory/bridging behaviors tend to have musculature dominated by Type I (slow-twitch) fibers (Schilling, 2005; Schmidt and Schilling, 2007; Kohn et al., 2011; Myatt et al., 2011; Curry et al., 2012). These sorts of relationships are unknown in mimetic musculature; however, a similar insight would be helpful in understanding how human facial expression muscles vary with respect to those of other primates and other mammals, the evolution of human facial expression and speech/language, and would even be useful in optimizing animal models of human disease, disorders, and associated surgical interventions such as Parkinson's disease, autism, and face transplants.
Animal models for most of these disorders and interventions use murids (rats and mice) or rhesus macaques. Previous studies have documented relatively great complexity in rhesus macaque facial displays and the corresponding mimetic musculature but not in rats/mice. It is largely unknown whether murids, or even rhesus macaques, represent adequate models of the complex function of human mimetic musculature and facial displays. By examining the aspects of mimetic musculature physiology and morphometrics at the microanatomical level, this study aims to address this question.
This study examines the relationship between fiber type characteristics and mimetic musculature function using a murid (the laboratory mouse, Mus musculus), an Old World monkey (the rhesus macaque, Macaca mulatta), and humans. The mouse and macaque are species often used as experimental models of human diseases, disorders, and in surgical interventions. They also represent broadly separated phylogenetic positions relative to one another and to humans, and they occupy varied social and ecologic niches relative to humans. Mice (Class Rodentia) are nocturnal, small-bodied (about 20 g), and can live in large social groups; however, they have not been documented to use facial expressions as a means of social communication. Instead, they rely heavily on olfactory communication and “face touch,” tactile sensory exploration via the vibrissae (e.g., Vander Wall et al., 2003; Wilson and Reeder, 2005; Merritt, 2010). Rhesus macaques are phylogenetically much closer to humans, are diurnal, medium-sized (about 7,700 g), live in complex, large groups, and, like humans, rely heavily on facial expression as a means of social communication but not, reportedly, to the same extent as in humans (Thierry, 1990, 2000; Fooden, 2000; Parr et al., 2010).
To better understand the physiological and morphological specializations at the microanatomical level associated with human mimetic musculature function, we test the following hypotheses related to mimetic muscle physiology.
Hypothesis 1: Fiber type proportions
Because of the frequent use of facial expressions of emotion in humans and to a lesser extent in rhesus macaques (Parr et al., 2010), we hypothesize that humans will have the significantly (P < 0.05) greatest proportion of fast-twitch fibers followed by rhesus macaques (human > macaque > mouse). Because facial expressions occur rapidly and last only a few seconds (Ekman and Friesen, 1982; Schmidt et al., 2003; Parr et al., 2010), we further hypothesize that there will be no significant difference (P > 0.05) among the groups in percentage of slow-twitch muscle fibers among groups.
Hypothesis 2: Fiber morphometrics
Because of the frequent use of facial expressions of emotion in humans and to a lesser extent in rhesus macaques (Parr et al., 2010), we hypothesize that humans will have significantly greater cross-sectional area, diameter, and length of fast-twitch fibers than macaques and macaques will have greater values than mice (human > macaque > mouse). Furthermore, we hypothesize that there will be no significant difference in cross-sectional area, diameter, and length of slow-twitch fibers (human = macaque = mouse). If mimetic muscle morphometrics are not adaptive but are instead influenced primarily by body size differences, then we hypothesize that there will be significant differences in morphometrics of slow-twitch fibers in all cases with humans > macaques > mice.