4278 The Journal of Experimental Biology 213, 4278-4290 © 2010. Published by The Company of Biologists Ltd doi:10.1242/jeb.047647 Functional morphology and three-dimensional kinematics of the thoraco-lumbar region of the spine of the two-toed sloth John A. Nyakatura* and Martin S. Fischer Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität, D-07743 Jena, Germany *Author for correspondence ([email protected]) Accepted 25 September 2010 SUMMARY Given the importance of thoraco-lumbar spine movements in the locomotion of mammals, it is surprising that in vivo three- dimensional (3-D) data on the intervertebral movement of the mammalian thoraco-lumbar vertebral column during symmetrical gaits is limited to horses and dogs. To test whether kinematic patterns similar to those published for these cursorial species are also present during a contrasting mode of quadrupedalism, we quantified thoraco-lumbar intervertebral movements, the resulting pelvic displacements and relative femoral movements during the trot-like steady-state suspensory quadrupedal locomotion of the two-toed sloth (Xenarthra, Choloepus didactylus). Scientific rotoscoping, a new, non-invasive approach that combines synchronous biplanar high speed X-ray videos and the reconstruction of skeletal elements from computed tomography bone scans, was used to quantify 3-D kinematics. An analysis of vertebral anatomy and epaxial muscle topography suggests that the thoraco-lumbar spine of sloths is well suited to producing lateral bending and long-axis rotation, but limits powerful sagittal extension. Sloths exhibit complex 3-D movements in the thoraco-lumbar spine that are comparable to those observed in other arboreal quadrupedal mammals. Monophasic lateral bending and long-axis rotation, biphasic sagittal bending and maximal amplitude of sagittal bending at the lumbo-sacral joint were also found in other quadruped mammals and may represent general aspects of mammalian symmetric gaits. Maximal amplitude of lateral bending and long-axis rotation vary in regard to the vertebral level. It is suggested that a cranio-caudal pattern of angular deflections of the spine results from the out-of-phase movement of diagonal forelimbs and hindlimbs in other walking gaits, because it is not evident in the trot-like locomotion analyzed here. The analysis also illustrates the difficulties that arise when lumbar movement is deduced from intervertebral joint morphology alone. Key words: intervertebral joint, vertebral column, XROMM, scientific rotoscoping, pelvis, femur, Choloepus didactylus, Xenarthra. INTRODUCTION morphology of the vertebrae (e.g. Slijper, 1946; Boszczyk et al., Movements of the vertebral column are of fundamental significance 2001). However, only a fraction of the possible in vitro mobility of in the locomotion of mammals, because they have been shown to the musculo-skeletal system or of the mobility at non-locomotor contribute significantly to propulsion (e.g. Howell, 1944). The most activities such as grooming, fighting or mating can be expected substantial movement of the vertebral column during symmetrical during cyclic locomotion (Fischer, 1998). Additionally, in at least gaits of mammals is a monophasic lateral bending that results in one available example of experimental in vivo motion analysis, the maximal lateral displacement of the pelvis to either side at touch- movements observed were greater than expected on the basis of the down of the hindlimb of the same side of the body (Shapiro et al., articular features (Haussler et al., 2001). 2001). Secondly, there occurs a less pronounced, biphasic sagittal Because 3-D intervertebral movements are difficult to observe, bending. Maximal sagittal flexion occurs at hindlimb touch-down necessitating 3-D in vivo methods, data relating to these movements whereas maximal extension occurs at hindlimb lift-off (Schilling have only been published for horses (Haussler et al., 2001) and, to and Fischer, 1999; Faber et al., 2000; Ritter et al., 2001; Licka et a limited extent, dogs (Wood et al., 1992; Schendel et al., 1995) – al., 2001). Thirdly, there is axial rotation about the long-axis of the both highly cursorial mammals adapted to sustained running. These spine, which is more pronounced in symmetrical gaits than in few studies relied on the invasive instrumentation of the vertebrae asymmetrical gaits (Faber et al., 2000). The pelvis is thus displaced analyzed. three dimensionally (3-D) during symmetrical gaits in mammalian In kinematic studies on the back movements of horses during a locomotion (cf. Jenkins and Camazine, 1977). slow lateral sequence walk, maximal intervertebral lateral bending In view of the importance of these 3-D axial movements in was observed to occur earlier between the lumbar vertebrae than mammalian symmetrical gaits, it is surprising that the kinematic between the more cranial thoracic intervertebral joints, whereas in data available on the body axis are limited. Although published a trotting gait this shift was not evident (Faber et al., 2000; Haussler quantifications of 3-D pelvic displacements during symmetric et al., 2001). Accordingly, Schilling and Carrier documented mammalian quadrupedalism are themselves scant (Jenkins and sequential electromyographical (EMG) activation patterns in the Camazine, 1977; Schilling and Fischer, 1999; Wennerstrand et al., back muscles of dogs during walking and galloping, but 2004; Schmidt, 2005), the minute intervertebral movements synchronized activity during trotting (Schilling and Carrier, 2010). associated with these displacements are even less well investigated. The authors concluded that the cranio-caudal EMG patterns of dogs Efforts have been made to deduce intervertebral mobility from the are consistent with a traveling wave of trunk bending in walking THE JOURNAL OF EXPERIMENTAL BIOLOGY Morphology and 3-D kinematics of sloth thoraco-lumbar spine 4279 gaits and with a standing wave of trunk bending in trotting gaits Anatomical investigation (Schilling and Carrier, 2010). Kinematic data and EMG data thus Anatomical investigation was undertaken on a female cadaver of imply a close relationship between footfall pattern and the 3-D C. didactylus donated by Dresden Zoo (Germany). After dissection movements of the vertebral column during symmetric gaits. to study the epaxial muscular topography, the cadaver was macerated Furthermore, published studies on the 3-D axial movement of and the vertebrae of the thoraco-lumbar spine were photographed quadrupedal mammals have shown that there are regional differences to document the intervertebral joint configuration of the two-toed in the magnitude and pattern of the three axial rotations: lateral sloth. In this paper we use the anatomical nomenclature of the bending about a dorso-ventral axis, sagittal bending about a latero- Federative Committee on Anatomical Terminology (FCAT, 2008). lateral axis and long-axis rotation about a longitudinal axis (Haussler The subjects used in the anatomical investigation and the motion et al., 2001). analysis (see below) have been used in previous studies and have If previously published patterns of 3-D axial movement during been shown not to have uncharacteristic morphologies. Their symmetric mammalian quadrupedalism are also present in a morphometric parameters were within 1 s.d. of a larger sample that contrasting type of symmetric locomotor behavior, they are likely was composed of museum material (Nyakatura and Fischer, 2010). to represent a more general pattern. To this end, we present here Neither the female [10.6kg, 87cm in length (measured from the an in vivo analysis of 3-D thoraco-lumbar intervertebral movements anterior tip of nose to the ischium)] nor the male (6.5kg, 78cm) during suspensory quadrupedal locomotion in the two-toed sloth displayed any peculiarities. (Xenarthra, Choloepus didactylus, Linné 1758). The following statements reflect what we would expect with regard to the Experimental setup for biplanar high-speed X-ray video movements in the thoraco-lumbar spine of the two-toed sloth during recordings suspensory quadrupedal locomotion on the basis of data available The experimental setup for obtaining synchronous biplanar X-ray on horses and dogs: videos was described in detail in a previous publication (Nyakatura 1. Lateral bending will be monophasic and maxima will occur et al., 2010). Briefly, we recorded synchronous, digital high-speed to either side associated with touch-down events of the hindlimbs. X-ray videos from the dorso-ventral and latero-lateral perspectives 2. Sagittal bending will be biphasic and maxima of flexion will during steady-state locomotion in two individuals (Fig.1). Both be associated with touch-down events of the hindlimbs, whereas 40cm diameter image intensifiers were equipped with a Visario minima will occur at instances of hindlimb lift-off. SpeedcamTM (Weinberger GmbH, Erlangen, Germany) and recorded 3. Long-axis rotation will be monophasic and maximal rotations at a resolution of 1536ϫ1024pixels and a frame rate of towards one side of the body will be associated with touch-down 300framess–1. Any distortion of X-ray images was corrected with of the ipsilateral hindlimb, whereas minima will occur at lift-off of the help of a MatlabTM workflow developed by the XROMM group the ipsilateral hindlimbs. (Brown University, Providence, Rhode Island, USA). Images were 4. Amplitudes of intervertebral angular deflections will be highest undistorted by recording the X-ray