Jaw kinematics and mandibular morphology in humans

Abstract

Understanding the influence of feeding behavior on mandibular morphology is necessary for interpreting dietary change in fossil hominins. However, mandibular morphology is also likely to have an effect on feeding behavior, including jaw kinematics. Here we examine the relationships between mandibular morphology and jaw kinematics in humans using landmark-based morphometrics to quantify jaw movement. Three-dimensional movements of reflective markers coupled to the mandible and cranium were used to capture jaw movements while subjects chewed cubes of raw and cooked sweet potato. Geometric morphometric methods were adapted to quantify and analyze gape cycle motion paths. Gape cycles varied significantly across chewing sequences and between raw and cooked sweet potato. Variation in gape cycle size and shape is related to the width (intergonial distance) and length of the mandible. These results underline the fact that jaw kinematic variation within and between taxa is related to and may be influenced by mandibular morphology. Future studies examining kinematic variation should assess the influence of morphological differences on movement.

Introduction

Although diet and mandibular morphology have been widely studied in primates, the relationships between them remain obscure (Hylander, 1979, Hylander, 1985, Hylander, 1988, Bouvier and Hylander, 1981, Smith, 1983, Bouvier, 1986a, Bouvier, 1986b, Daegling, 1992, Cole, 1992, Ravosa, 1996, Ravosa, 2000, Taylor, 2002, Taylor, 2006, Vinyard et al., 2003). One possible reason may be that diet only influences mandibular morphology indirectly through variation in gross aspects of feeding behavior (Ross et al., 2012). In turn, feeding behavior is variably impacted by several aspects of diet, including food geometric and material properties, as well as by an animal's phylogenetic, ecological and sociological context (e.g., Hylander, 2013). However, there is also evidence that, in humans at least, the direction of causality may in some cases be the reverse of what is traditionally assumed: i.e., mandibular morphology may affect various aspects of feeding behavior, including EMG activity and jaw kinematics (Ahlgren, 1966, Møller, 1966, Ingervall and Thilander, 1974, Ingervall and Helkimo, 1978, Kiliaridis et al., 1985). This paper presents a detailed analysis of relationships between mandibular morphology and jaw kinematics in humans using a novel application of geometric morphometric techniques to kinematics.

A chewing sequence is the sequence of gape cycles from ingestion to swallow and can be divided into sequentially numbered cyclic jaw movements or gape cycles (Fig. 1). The kinematics of the gape cycle are typically measured by tracking vertical and lateral displacement of the jaw over time (e.g. Reed and Ross, 2010, Iriarte-Diaz et al., 2011, Laird, 2017). Vertical displacement of the jaw during gape cycles is thought to vary as chewing progresses within a sequence reflecting the breakdown of food particles, bolus formation, changes in external bolus properties, and changes in food material properties (Foster et al., 2006, Woda et al., 2006, Vinyard et al., 2008). In this context, decreases in vertical displacements and variation in muscle activity amplitudes through the chewing sequence reflect the decrease in food fragment sizes and variation in bolus properties as the sequence progresses (Pruim et al., 1978, Manns et al., 1979, Hylander and Johnson, 1985, Spencer, 1998, Olmsted et al., 2005, Vinyard et al., 2008, Reed and Ross, 2010, Laird, 2017). In humans, foods with higher toughness are often associated with greater vertical and lateral jaw displacements during the gape cycle (Anderson et al., 2002, Foster et al., 2006, Wintergerst et al., 2008, Laird, 2017; but see; Takada and MiyawakiTatsuta, 1994, Peyron et al., 1997, Reed and Ross, 2010).

What has seldom been addressed is the possibility that jaw kinematics are also impacted by the overall shape of the mandible. This is of interest because variation in a suite of features of human mandibular morphology, particularly differences in symphyseal height, overall anteroposterior length, mediolateral breadth, and the gonial angle, has been associated with geographic, climatic, dietary, and feeding performance factors (Kaifu, 1997; Nicholson and Harvati, 2006; von Cramon-Taubadel, 2011; Katz et al., 2017). When modeled as a constrained lever, variation in the length of mandible will move the dental functional area relative to the muscle resultant and change the location of maximum bite force production (Greaves, 1978, Spencer and Demes, 1993). Large vertical bite forces are associated with a short and broad mandibular ramus, a low coronoid process/shallow mandibular notch, and large bicondylar breadth (Herring and Herring, 1974). Humans with longer faces, narrower mandibles, and larger gonial angles have reduced masseter muscle thickness (Throckmorton et al., 1980, Kiliaridis and Kälebo, 1991; Van Spronsen et al., 1992). These features are thought to influence the mechanical advantage of the primary jaw adductors -- the masseter and temporalis muscles.

However, there is a well-documented trade-off between mechanical advantage and gape such that larger gapes require greater muscle stretch and/or posteriorly positioned jaw elevator muscles, negatively impacting jaw mechanical advantage (Herring and Herring, 1974, Lindauer et al., 1993, Van Eijden and Turkawski, 2001, Hylander, 2013, Iriarte-Diaz et al., 2017). This indicates that vertical movements of the jaw that stretch the muscles beyond their optimum length result in decreased mechanical advantage and lower bite forces. Beyond this, the ontogeny of the mandible is well known to be strongly influenced by its loading history (Moss and Salentijn, 1969, Pearson and Lieberman, 2004), hence an association between function and mandibular size and shape is to be expected.

We tested a series of hypotheses to investigate how gape cycle size and shape vary with cycle number across a chewing sequence, food type, and measures of mandibular morphology. First, gape cycles were hypothesized to change across the chewing sequence (H1), such that gape cycles are larger at the beginning of the chewing sequence before the food has been broken down. Gape cycles were also expected to differ between food types (in this case raw and cooked sweet potato) within each subject, reflecting differences in food particle breakdown, toughness, and elastic modulus. We hypothesized that raw sweet potato gape cycles will be larger than cooked sweet potato gape cycles, reflecting food material property-related differences in rates of particle breakdown and swallow-safe bolus formation (H2). Next, we compared jaw kinematics across individuals, assessing the extent to which gape cycle variation with food type and cycle number is consistent across individuals (H3). Finally, we hypothesized that differences in gape cycles among individuals covary with measures of mandibular size and shape (H4). Specifically, we hypothesize that smaller gape cycles are associated with greater mandibular mechanical advantage and tradeoffs between gape and bite-force. Smaller gape cycles would allow subjects to maximize their mechanical advantage and minimize muscular stretch. As there are likely three-dimensional complexities of jaw movement that can only be quantified and analyzed using multivariate techniques, we addressed these hypotheses using a novel application of geometric morphometric techniques to gape cycles. This allows us to quantify and compare the three-dimensional size and shape of these motions to better understand how cycle size and shape vary with cycle number, food, and morphology.