Locomotor head movements and semicircular canal morphology in primates

Abstract

Animal locomotion causes head rotations, which are detected by the semicircular canals of the inner ear. Morphologic features of the canals influence rotational sensitivity, and so it is hypothesized that locomotion and canal morphology are functionally related. Most prior research has compared subjective assessments of animal "agility" with a single determinant of rotational sensitivity: the mean canal radius of curvature (R). In fact, the paired variables of R and body mass are correlated with agility and have been used to infer locomotion in extinct species. To refine models of canal functional morphology and to improve locomotor inferences for extinct species, we compare 3D vector measurements of head rotation during locomotion with 3D vector measures of canal sensitivity. Contrary to the predictions of conventional models that are based upon R, we find that axes of rapid head rotation are not aligned with axes of either high or low sensitivity. Instead, animals with fast head rotations have similar sensitivities in all directions, which they achieve by orienting the three canals of each ear orthogonally (i.e., along planes at 90°angles to one another). The extent to which the canal configuration approaches orthogonality is correlated with rotational head speed independent of body mass and phylogeny, whereas R is not.angular velocity | vestibular T he inner ear contains three bony semicircular canals, each of which encloses an endolymph-filled duct. Head rotations during locomotion cause inertial endolymph movements that are communicated to the brain. Canal morphology affects endolymph flow and thus influences an animal's sensitivity to rotation; if an animal is more sensitive to rotations about some axes than others, and if different patterns of head rotation are produced by different locomotor behaviors, then canal morphology and locomotion could be functionally related. By this reasoning, differences in canal morphology in living and extinct animals have been attributed to interspecific differences in locomotion (1-10), but characterization of any functional relationship between canal morphology and locomotion has been limited by the use of simplified models of canal sensitivity and the absence of in vivo data about how the head actually moves (11).The relevant variables for comparing canal sensitivity with head movement are angular velocity vectors and vestibular sensitivity vectors, respectively. (Although the direct stimulus to the canal is angular acceleration, the canal response is proportional to angular velocity within a range of head movement frequencies. Angular velocity was used here for a variety of reasons, as described in SI Materials and Methods.) Angular velocity vectors characterize instantaneous head rotations about different axes and can be experimentally measured in moving animals. Vestibular sensitivity vectors characterize the extent to which an animal is more sensitive to rotations about some axes than other axes. Although vestibular sensitivity vectors cannot be measured directly, t...

Digital reconstruction of the inner ear of Leptictidium auderiense (Leptictida, Mammalia) and North American leptictids reveals new insight into leptictidan locomotor agility

“…Recent investigations of 3D kinematic experiments and angular arrangement of the semicircular canals in primates show that the angles of the canal planes are highly correlated with sensitivity and fast head rotations, and therefore locomotor agility (Malinzak et al 2012).…”

“…Thus, we calculated the variance from 90°among angles between the three semicircular canals [90var = (sum of (n) squared deviations from 90°)/(n-1)], in order to estimate possible corresponding patterns of head rotation and locomotor agility within Leptictida, independently from body mass (Malinzak et al 2012).…”

“…However, in being 105.4°, this angle is clearly larger than 90°, but the resulting log 10 90var of 2.09 is pretty close to that of Leptictis (Table 1). A plot of the investigated Leptictida in the ''primate regression analysis'' (log 10 90var versus log 10 AVM) of Malinzak et al (2012) indicates that Palaeictops would have a much higher head angular velocity magnitude (AVM) than the other two leptictidans, even higher than almost all primates of that study (Fig. 6a).…”

“…Following Malinzak et al (2012), we also estimated the rotational head speed as a proxy for locomotor agility. The planes between the semicircular canals in Leptictidium all form angles that are lower than 90° (Table 1).…”

“…Besides postcranial anatomy, the shape and proportions of vestibular labyrinth structures also record configurations related to locomotion and posture, which in turn can be used as a reliable proxy to characterise locomotor behaviour and agility in extant, and, by extrapolation, extinct mammals (e.g., Spoor et al 2007;Walker et al 2008;Silcox et al 2009;David et al 2010;Macrini et al 2010;Malinzak et al 2012;Ryan et al 2012;Berlin et al 2013). To date, nothing is known about this pattern in Leptictida.…”