This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and

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1 This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier s archiving and manuscript policies are encouraged to visit:

2 The Veterinary Journal 198 (2013) e70 e74 Contents lists available at ScienceDirect The Veterinary Journal journal homepage: Development of postural balance in foals Sandra Nauwelaerts, Sara R. Malone, Hilary M. Clayton McPhail Equine Performance Center, Michigan State University, East Lansing, MI, USA article Keywords: Equine Postural sway Balance control Stability Center of pressure info abstract This study used stabilographic analysis to measure and describe changes in stability during standing in foals from birth to 5 months of age. Stabilographic analysis was performed on newborn foals immediately after first suckling then daily until 1 week of age, weekly until 1 month of age and monthly until 5 months of age. Ground reaction force (GRF) data were collected for periods of 8 s with the foal standing on one or two force plates recording at 1000 Hz. Stabilographic variables describing the, and of center of pressure (COP) movements were derived from the GRF data. Amplitudes, which were initially larger in the craniocaudal direction, decreased over time in both directions, with craniocaudal becoming smaller than mediolateral by 1 2 months of age. At birth, COP was larger in the craniocaudal direction, but decreased rapidly to become smaller than mediolateral by 3 months of age. Mean at birth was higher craniocaudally, but became similar in both directions at 2 months of age. The rapid reductions in craniocaudal and were thought to reflect improvements in strength and coordination of the flexor/extensor musculature. Newborn foals splay their limbs to compensate for poor control of the abductor/adductor musculature and, after the limbs assumed a vertical posture, mediolateral sway increased. Ó 2013 Elsevier Ltd. All rights reserved. Introduction Horses are precocial, which means that their young are relatively mobile at birth. Foals stand up within a few hours after birth to suckle. Neonates of precocial species have been described as having righting reflexes and displaying adult-like postural abilities and coordination (Fox, 1964; Lelard et al., 2006). Research on development of motor control has mainly focused on altricial species. The assumption of adult-like features might explain why the development of postural ability in precocial species has been understudied, but this assumption has never been explicitly tested. Postural balance is defined as the ability to stand in a comfortable posture with minimal movements of the body segments. In order to maintain static balance, the body s center of mass (COM) must be maintained within the limits of the base of support, which are determined by the contacts with the ground. Mechanically, balance is achieved by counteracting gravitational forces on the COM with ground reaction forces (GRF) under the feet. The COM moves constantly and these movements are monitored by visual, vestibular and somatosensory receptors (Forssberg and Nasher, 1982). The sensory input guides the muscular response, resulting in changes in the GRF distribution beneath the feet. These GRFs can be measured using one or more synchronized force plates. Movements of the body s center of pressure Corresponding author. Tel.: address: sandra.nauwelaerts@ua.ac.be (S. Nauwelaerts). (COP), calculated as the position of the origin of the resultant of the vertical GRF, can be plotted in the horizontal plane as a stabilogram. Derived stabilographic variables quantify performance of the postural balance system. Development of postural control requires maturation of the nervous and musculoskeletal systems and the interaction between them (Massion, 1992). It takes almost a year before human infants are able to stand independently and many additional years are required for them to develop adult-like postural control (Chen et al., 2008; Wu et al., 2009) using a combination of open-loop and closed-loop mechanisms (Collins and DeLuca, 1993). Closed-loop control is monitored by sensory feedback, while open-loop control involves ballistic correctional movement, the effectiveness of which is not known until after the movement has occurred (Riach and Starkes, 1994). Younger children appear to rely on fast but imprecise ballistic control, with a gradual change at 4 7 years of age to a more adaptable sensory feedback correction strategy. This is associated with reductions in both sway and that are independent of changes in height and weight (Riach and Starkes, 1994). In sharp contrast to the body of knowledge describing the development of balance in children, little is known about development and maturation of balance in foals, which differ in several ways from human infants. The precocious development of the musculoskeletal system allows foals to stand and move at rapid speed within a few hours after birth (Adams and Mayhew, 1984; Acworth, 2003). The rectangular base of support is long /$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.

3 S. Nauwelaerts et al. / The Veterinary Journal 198 (2013) e70 e74 e71 craniocaudally (CC) and short mediolaterally (ML), which is the opposite of the relative dimensions of the human base of support. It seems reasonable to assume from the size and shape of the base of support that balancing strategies of a foal will differ from those of a biped. This study quantified the postural balance of newborn foals and measured changes in stabilographic variables during the early days, weeks and months of life. The experimental hypothesis was that, even in this precocial species, values of stabilographic variables representing the, and of COP movements will decrease with age. Materials and methods Subjects The subjects were 12 Arabian foals that had a normal gestation and parturition. After birth, the foals were allowed to stand and suckle the mare undisturbed. After suckling, each foal was carried to the force plate, which was positioned just outside the doorway to the foaling stall. The foal was oriented facing the mare that observed the procedure and was restrained about 1 m from her foal (Fig. 1). During data collection, one or two handlers stood close to the foal, but without any direct contact with the foal s body. After collecting force data, the foal was returned to the stall. On subsequent occasions, the foal was either carried or walked to the force plate for data collections. From birth until each foals was 2-months-old, data were collected using a single force plate. From 3 months of age onwards, two synchronized force plates were used to accommodate the larger base of support of the growing foals. In accordance with the normal management practices at the farm, each mare was turned out with her foal daily (9.00 am to 3.00 pm) in individual paddocks during the first week. The mare and foal were then turned out full-time in a large pasture with a group of mares and foals. The foals hooves were trimmed at 6 week intervals starting at 2 months of age. Data collection Postural stability was measured using two Bertec FP6090 force plates (Bertec Corporation) with 600 mm 900 mm 150 mm top plates, each with 900 kg load capacity recording at 1000 Hz. Each force plate had a 16-bit digital internal amplifier, with embedded calibration information to reduce cross-talk between channels. The force data were fed through a digital AM6800 amplifier (Bertec Corporation) connected to a laptop. Forces and moments applied to the force plate were measured in three dimensions. During data recording, the foals had to stand motionless without stepping or visual movement of the head and neck. A digital camcorder was positioned on the lateral side of the force plate to enable qualitative screening of the trials. Data were recorded on the day of birth, daily for the first week, weekly for the first month and monthly until the foals were weaned at 5 months of age. Each phase of data recording consisted of at least three trials, each with a minimal duration of 10 s. The duration of the trials was standardised to 8 s. Movements of the COP of the resultant GRF were calculated and displayed in a stabilogram. The origin of the stabilogram was defined as the mean value of all data points in the craniocaudal (CC) and mediolateral (ML) directions, which corresponded with the longitudinal and transverse axes of the force plate(s). CC and ML s of the COP were determined from the stabilogram as the differences between maximal and minimal values in the two perpendicular horizontal directions. CC and ML velocities of the COP (mean and standard deviation) were calculated as the first derivative of the COP position in the CC and ML directions, respectively, through time. Fast Fourier transformation was used to determine mean power. The foal s weight was the average vertical force during the trial. Statistical analysis The data were linearized by log transformation and the transformed data were analysed using a mixed model ANOVA. Each trial was used as a separate measurement and no averaging was performed. Relationships between sway s and velocities were examined using Pearson s product moment correlation. All statistical tests were based on a probability of P < Fig. 1. Foal standing on a single force plate in preparation for data collection. During recordings, the handler stood close to the foal but had no physical contact with it. Results Body weights of the foals increased through the period of study (Fig. 2). Sway s were initially larger in the CC direction Table 1 Mean stabilographic variables (, and in the craniocaudal and mediolateral directions) from birth to 15 months of age (n = 12) with Tukey-B groupings. Days after birth Craniocaudal Group CC Mediolateral Group ML Craniocaudal Group CC Mediolateral Group ML Craniocaudal Group CC Mediolateral /2 53 1/ /2 23 2/ /3 53 1/2 24 2/ /3 21 2/ /3 21 2/3 46 1/ /3 23 2/ /2 21 2/ / / / / / / / / Days with the same Tukey B group numbers do not differ significantly from each other. Only days belonging to separate groups without overlap differ significantly. Group ML

4 e72 S. Nauwelaerts et al. / The Veterinary Journal 198 (2013) e70 e74 Fig. 2. Mean ± standard deviation of body weight of foals (n = 12) during the first 5 months of age. but they decreased progressively over time in both directions (Table 1). The decrease in sway was more rapid in the CC direction and it became smaller than ML by 2 months of age. Results of ANOVA (Fig. 3) showed that, although CC decreased rapidly over the first month, the data were grouped into several overlapping subsets (Table 1). There were significant decreases at 2 and 3 months of age, after which CC did not change. For ML, there were no significant differences between days of the first week, but significant decreases occurred at 2 weeks and 4 months of age (Fig. 3). The standard deviations for both CC and ML s were largest immediately after birth and decreased markedly over time. Stabilograms from one foal from birth to 5 months of age are shown in Fig. 4. At birth, CC was considerably higher than ML, but it decreased significantly at 2 weeks, 3 weeks, 2 months and 3 months of age, by which time it was lower than ML. Mediolateral was significantly higher on day 0 than on any other day. The post hoc tests grouped the values into over-lapping subsets during the remainder of the first week of age, then showed significant decreases from 2 weeks to 2 months of age, after which the values increased again in the third and fourth months of age (Fig. 3). Initially, mean frequencies were higher in the CC direction and the values showed little change over time. In the ML direction, frequencies did not change over the first 2 months of age, after which they became higher than in the first month. At 5 months of age, CC and ML frequencies were similar. Standard deviations for the measurements remained high throughout the study. Fig. 3. Mean ± standard deviation for the stabilographic variables describing (A and B), (C and D) and (E and F) in the craniocaudal (filled circles, right panels) and mediolateral (open circles, left panels) directions from birth to 15 months of age (n = 12). Results of the ANOVA and Tukey B post hoc tests are shown above each graph. Note that data points for CC and ML are similar in magnitude at 2 months and error bars for CC and at 3, 4 and 5 months are smaller than the diameter of the data points.

5 S. Nauwelaerts et al. / The Veterinary Journal 198 (2013) e70 e74 e73 Fig. 4. Typical stabilograms of one example foal from birth to 5 months of age. The first trial recorded on each day is shown after trimming the data to 8 s duration and all stabilograms are shown with the same scaling on both axes, which is shown on the first stabilogram. The CC and ML s and velocities were correlated with each other (: r = 0.734; : r = 0.645) and, in each direction, s was correlated with (CC: r = 0.760; ML: r = 0.848). Discussion This study has shown large age-related reductions in and of COP movements in the CC direction, and smaller changes in the ML direction, which supports the experimental hypothesis. The patterns of change in and were similar, which is not surprising, since these variables were correlated, as they are in human beings (Riach and Starkes, 1994). Even though sway and decreased rapidly in the first 2 weeks after birth, significant decreases could still be detected after 3 months of age. Foals are able to stand unaided soon after birth and to move in a coordinated manner shortly thereafter. Foals usually stand within 2 h postpartum and are sufficiently well balanced to nurse soon afterwards (Adams and Mayhew, 1984; Acworth, 2003). Early ingestion of colostrum is necessary for passive transfer of immunoglobulins (Raidal et al., 2005), so foals in this study were not disturbed until after they had suckled. Neonatal foals are less aware of and less responsive to external stimuli than older foals, and this facilitated data collection. When restrained firmly with one arm around the chest and the other around the rump, neonatal foals become relaxed and almost cataplectic (Adams and Mayhew, 1984). This response facilitated placing foals on the force plate during the early days of life. Additionally, foals are not born with a full set of reflex responses. For example, the menace reflex develops during the first 2 weeks postpartum (Adams and Mayhew, 1984). By the time these reflexes were present, the foals were already accustomed to standing on the force plate and accepted it without resistance. Our results indicate that newborn foals were initially quite unstable, as shown by the relatively large values of COP and, which are indicative of poor postural control. However, the magnitudes of these variables decreased rapidly over the first week of life and then more slowly over the following weeks and months as muscular strength and neuromotor control improved. Children show a change in strategy from open-loop control to closed-loop control at 7 8 years of age (Riach and Starkes, 1994). In closed-loop control, COP movements are monitored by sensory feedback and the inherent time delay in processing the feedback by the central nervous system results in slower COM (Riach and Starkes, 1994). We suggest that neonatal foals, with their incompletely developed neuromuscular reflexes, weak musculature and inexperience in postural control, rely on open-loop control, but over the first 2 weeks of life they learn to integrate sensory input and change to a closed-loop mechanism, with consequent reductions in COP and. COP, and were all higher in the CC direction initially, but became lower in the CC than the ML direction by 3 months of age. This may be related to the fact that equine limbs have evolved to move primarily in a parasagittal plane, which implies a large range of motion in flexion extension. In accordance with the need to move and stabilise the joints in the parasagittal plane, the flexor/extensor musculature is well developed, although not fully functional immediately after birth. In the postnatal period, the musculature develops and hypertrophies, which affects postural stability during standing. Furthermore, the equine base of support has its longer dimension craniocaudally, which allows the COM to move farther in this direction without risk of falling. Consequently, the fact that COP and were initially larger in the CC direction may reflect laxity in control in this direction, since the COM can migrate farther without leaving the base of support. Reduction of CC sway in this direction likely accompanies the development of co-contraction in flexor and extensor muscles, resulting in increased joint stiffness, which has the effect of stabilizing the body in the sagittal plane (Wang et al., 2006). A further indicator of maturation of the musculoskeletal system is that the gaits, which initially are stilted and hypermetric, become better coordinated within a few days after birth (Adams and Mayhew, 1984). We hypothesize that improved coordination skills, combined with increasing strength of the flexor extensor musculature with age, stiffened the joints, which damped the sagittal plane movements and thus decreased CC sway and. The equine base of support is narrow in the ML direction and has a relatively small abductor and adductor muscle volume to provide stability in this direction. Newborn foals splay their limbs (Adams and Mayhew, 1984; Acworth, 2003), which increases the width of the base of support and may assist in maintaining the COM within the lateral boundaries. Adoption of a splayed posture may also facilitate using the extrinsic limb musculature to adjust ML forces and sway patterns. Abduction and adduction are possible at the distal interphalangeal, hip and shoulder joints. Collateralmotion of the distal interphalangeal joints allows the hoof to remain flat on the ground with the limb abducted (Chateau et al., 2002), while the shoulder and hip joints allow limb abduction relative to the trunk. With the elbow, carpal and metacarpophalangeal joints, or the stifle, tarsal and metacarpophalangeal joints, aligned in the frontal plane, the limbs act as struts to resist transverse movements of the body. Consequently, with the limbs fixed in this orientation, ML and were relatively small in neonatal foals. As in the CC direction, improvements in strength

6 e74 S. Nauwelaerts et al. / The Veterinary Journal 198 (2013) e70 e74 and coordination allow the extrinsic musculature to take over the function of providing mediolateral stability, with the limbs becoming more vertically oriented in older foals. ML started to increase at 2 months of age and became significantly higher from 3 months of age onwards compared with the first month. It has been reported that a higher of the COP may be indicative of a more responsive postural control system. Perhaps the smaller ML dimension of the base of support, combined with the smaller volume of abductor adductor musculature, requires a more dynamic postural response in this direction, resulting in a switch to an open-loop ballistic control strategy, as described by Riach and Starkes (1994). Although parts of the postural control system are functional at birth in precocious species such as the horse, the more complex motor patterns used to respond to perturbations still need to undergo maturation. In children, stereotyped, automatic postural adjustments are controlled by inherent central networks, while the incorporation of sensory input is considered to require a higher level of control and a learned ability (Forssberg and Nasher, 1982). This may also be true in horses. Average sway was low in newborn foals (<1 Hz), and decreased further with age. The average is close to that of their respiratory rate ( Hz). In humans, synchronization between respiration and postural sway has been observed (Schmid et al., 2004). Both heartbeat ( Hz in foals) and respiratory movements can cause small perturbations to the system that have to be dampened out to retain stability. When performing stabilography in adult horses, size can be represented by body weight (data not shown), but this is not necessarily true in growing foals because size, morphology and neuromuscular control strategies are all changing rapidly during the first few months of life. The foals in this study showed a fourfold increase in body weight during the first 5 months of life, but it is likely that changes in weight were accompanied by other changes in morphology (Anderson and McIlwraith, 2004; Splan et al., 2007), including increases in muscle mass, bone mass and segmental lengths. Consequently, data from foals are not directly comparable with those of adult horses. Even so, by 5 months the stabilographic variables of foals were within the range observed in adult horses (Clayton and Nauwelaerts, 2012). Therefore, even though the foal was still considerably smaller than an adult horse, their stabilogram variables were in the same order of magnitude suggesting that asymptotic values were reached by 5 months of age. The ideal duration for recording stabilographic data has not been determined in adult horses or in foals. In human beings, many studies use 30 s data collections, but this is difficult to achieve even in adult horses that have been trained to stand still. Since horses are a prey species, they tend to be alert and attentive to their surroundings, which may impose limits on the duration of data collection, even in a quiet environment. Previous equine studies have used durations of 10 s (Clayton et al., 2003; Bialski et al., 2004) or a variable duration in the range of s when the goal was to maximize variability in the data (Clayton and Nauwelaerts, 2012). The 8 s period of data collection was achieved by all foals at all time points and can be used to make comparisons within the same group of animals over time, but the results should not be compared directly with values of adult horses recorded over different sampling durations. Conclusions This study presents the first stabilographic data in foals and tracks the longitudinal development of equine balance during the early months of life. There were some obvious challenges involved in data collection, notably the fact that young foals are completely untrained and unfamiliar with any of the techniques used, but the immaturity of the neuromusculoskeletal system compensates to a certain extent by making the foals more compliant. The and of COP movements of newborn foals were relatively high, especially in the CC direction. The values decreased rapidly during the first week of life and then more slowly until 2 3 months of age, by which time they were more stable in the CC direction than the ML direction. However, COP showed relatively small changes during the first 5 months of a foal s life. Conflict of interest statement None of the authors of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper. Acknowledgements The authors wish to thank Rachel Buchholz, Whitney Allen, Erin Tans, Patricia Miyashiro, Emily Compton and Kyle McAleenan for assistance with the experiments and Paula Hitzler for supporting the study at the MSU Horse Teaching and Research Center. This study was supported by the McPhail endowment. References Acworth, N.R.J., The healthy neonatal foal: Routine examinations and preventative medicine. Equine Veterinary Education 6, Adams, R., Mayhew, I.G., Neurological examination of newborn foals. Equine Veterinary Journal 16, Anderson, T.M., McIlwraith, C.W., Longitudinal development of equine conformation from weanling to age 3 years in the Thoroughbred. Equine Veterinary Journal 36, Bialski, D., Lanovaz, J.L., Bohart, G.V., Mullineaux, D.R., Clayton, H.M., Effect of detomidine on postural sway in horses. Equine and Comparative Exercise Physiology 1, Chateau, H., Deguerce, C., Jerbi, H., Crevier-Denoix, N., Pourcelot, P., Audigie, F., Pasqui-Boutard, V., Denoix, J.-M., Three-dimensional kinematics of the equine interphalangeal joint: Articular impact of asymmetric bearing. Veterinary Research 33, Chen, L.-C. et al., The development of infant upright posture: sway less or sway differently? Experimental brain research 186, Clayton, H.M., Bialski, D., Lanovaz, J.L., Mullineaux, D.L., Reliability of a technique to measure postural sway in horses. American Journal of Veterinary Research 64, Clayton, H.M., Nauwelaerts, S., Is a single force plate adequate for stabilographic analysis in horses? Equine Veterinary Journal 44, Collins, J., DeLuca, C., Open-loop and closed-loop control of posture: A random walk analysis of center-of-pressure trajectories. Experimental Brain Research 95, Forssberg, H., Nasher, L.M., Ontogenetic development of postural control in man: Adaptation to altered support and visual conditions during stance. Journal of Neuroscience 2, Fox, M.W., Phylogenetic analysis of behavioral neuro-ontogeny in precocial and non-precocial mammals. Canadian Journal of Comparative Medicine and Veterinary Science 28, Massion, J., Movement, posture and equilibrium: Interaction and coordination. Progress in Neurobiology 38, Lelard, T., Jamon, M., Gasc, J.-P., Vidal, P.-P., Postural development in rats. Experimental Neurology 202, Raidal, S.L., McTaggart, C., Penhale, J., Effect of withholding macromolecules on the duration of intestinal permeability to colostral IgG in foals. Australian Veterinary Journal 83, Riach, C.L., Starkes, J.L., Velocity of centre of pressure excursions as an indicator of postural control systems in children. Gait and Posture 2, Schmid, M., Conforto, S., Bibbo, D., D Alessio, T., Respiration and postural sway: Detection of phase synchronizations and interactions. Human Movement Science 23, Splan, R.K., Denham, S.F., Staniar, W.B., Growth and conformation changes in warmblood horses from birth to two years of age. In: Proceedings of the 20th Equine Science Society Symposium, Baltimore, Maryland, USA, 5 9 June Abstract 104. Wang, Y., Asaka, T., Zatsiorsky, V.M., Latash, M.L., Muscle synergies during voluntary body sway: Combining across trials and within-a-trial analyses. Experimental Brain Research 174, Wu, J., McKay, S., Angulo-Barroso, R., Center of mass control and multisegment coordination in children during quiet stance. Experimental brain research 196,