Navigation – Plan du site

AccueilVolumes12Dossier spécial - BipédieS chez l...A baboon walking on a treadmill: ...

Dossier spécial - BipédieS chez les Primates : de la philosophie au comportement

A baboon walking on a treadmill: the use of positive reinforcement techniques to study bipedal walking in non-human primates

Un babouin se déplaçant sur un tapis roulant : utilisation des techniques de renforcement positif pour l'étude de la marche bipède chez les primates non-humains
François Druelle et Pablo Molina-Vila

Résumés

À ce jour, l'utilisation de techniques dites de renforcement positif pour étudier la locomotion des primates non humains reste peu développée. Cependant, l'utilisation d'animaux coopératifs qui peuvent se déplacer librement dans une configuration expérimentale nous permet de collecter des données précieuses et pertinentes, les rendant ainsi reproductibles et comparables entre les espèces. Sur la base des connaissances actuelles et de notre expérience, nous présentons ici une approche expérimentale qui vise à atteindre les standards de l'étude du mouvement humain chez un primate non humain, le babouin olive, Papio anubis, grâce à l'utilisation de techniques de renforcement positif. Ce rapport documente le protocole d’entraînement que nous avons mis en place à la Station de Primatologie du CNRS (France). Nous développons également l'importance de mener de telles expériences pour une meilleure compréhension du comportement bipède chez les primates non humains. Les études expérimentales qui incluent des animaux coopératifs pouvant se déplacer librement sont susceptibles de représenter des outils expérimentaux précieux pour combler d'importantes lacunes dans les connaissances sur la locomotion en général, et en particulier sur l'acquisition de la marche bipède habituelle au sein de la lignée humaine.

Haut de page

Notes de la rédaction

Received 15/06/2021, accepted after revisions 28/02/2022, published online 10/03/2022 in the context of the special issue "BipedalismS in Primates" (Varia 2021).

A translated version, in French, is available online.

Une version, traduite en français, est disponible en ligne.

Texte intégral

1 Introduction

1The way humans walk and run bipedally is unique and this adaptation represents a key milestone in the evolutionary pathway of our lineage (Alexander, 2004; Crompton et al. 2008; Pontzer, 2017). Today, bipedal walking and running can be studied with extreme accuracy thanks to many technological developments [e.g. accelerometers, force plates, surface electromyography (EMG) electrodes, optoelectric imaging systems]. As a result, bipedalism in humans is well described biomechanically, neurologically and physiologically (Kirtley, 2006; Winter, 2009) and these fields keep delivering fundamental findings and highly detailed results (e.g. Charles et al. 2021; Esrafilian et al. 2020; Wu et al. 2019). However, understanding the origin of habitual bipedal locomotion requires work on comparative models that are phylogenetically closely related to humans (e.g. O'Neill et al. 2018). The study of non-human primates and of the nature of their (occasional) bipedal locomotion represents a great opportunity to highlight the constraints related to this mode in non-adapted bipeds. However, studying bipedal locomotion in non-human primates using the same methodology as in humans represents a great challenge. The constraints of bringing a non-human primate into a laboratory to make it walk on a technical platform for biomechanical analysis and equipped it with sensors and markers are high, and obviously much higher than when studying humans (Fig. 1). For example, trying to make a non-human primate wear tiny infrared lights on a set of anatomical landmarks remains extremely challenging and there is always a high risk of having the expensive system destroyed by the animal.

2In this note, we propose documenting an experimental approach that aims at reaching the standards of the study of human movement in a non-human primate, the olive baboon, Papio anubis, thanks to the use of positive reinforcement techniques. We are applying this protocol in the context of our ongoing research work on the ontogeny of bipedal locomotion in baboons.

Figure 1

Figure 1

Illustrations showing a human individual equipped with a motion capture system with EMG to study knee joint loading and a baboon standing bipedally in a flexed posture. The illustration of the human individual was extracted from Esrafilian et al. (2020). The illustration on the right-hand side was taken by FD and shows a baboon raised in captivity at the primatology station of the CNRS.

2 Basic historical elements of the study of bipedal walking in non-human primates

3Locomotor resemblances and differences between human and non-human primates are of great interest in the field of palaeoanthropology. The first comparative and quantitative studies of human versus non-human primate bipedalism can be found in the pioneering works of Elftman and Manter (1944; 1935). In these studies, they used an advanced setup to quantify the distribution of pressure under the foot in a chimpanzee and a human walking bipedally. Forty years later, other experimental works opened new ways to explore the bipedal locomotion of non-human primates, laying the foundations of the modern comparative study of human bipedal walking (e.g. Ishida et al. 1974; Jenkins, 1972; Kimura et al. 1979; Prost, 1967; Stern & Susman, 1981; Taylor & Rowntree, 1973; Tuttle et al. 1979). These studies have highlighted both the differences and similarities between human and non-human primate bipedalism. For instance, the hyperextension of the hip at heel off and the straightened knee joint at the beginning of the stance phase are typical features of the human erect bipedalism that are not present in non-human primates (Ishida et al. 1974). Jenkins (1972) showed that, in chimpanzee, the femur is abducted and kept in a flexed position (as during quadrupedal knuckle-walking) and the movement of the pelvis is different from that of humans as it rises on the side of the swing leg (e.g. Thompson et al. 2021). There are also larger mediolateral displacements of the centre of mass in non-human primates walking bipedally compared to humans. On the other hand, Stern and Susman (1981) have shown that the role of the gluteus medius is the same in humans and great apes walking bipedally. Its role is to balance the side-to-side movement of the trunk at the hip during bipedal locomotion. Furthermore, Ishida et al. (1974) showed that both humans and chimpanzees present an extension of knee joint, significant activity of the gastrocnemius muscle, and a high peak of the vertical ground reaction force during the second phase of the stance phase.

4Since then, various setups have been developed and these have opened new perspectives about our understanding of human locomotor evolution (e.g. Aerts et al. 2000; Berillon et al. 2010; D'Août et al. 2004; Hirasaki et al. 2004; Hirasaki et al. 2006; Nakatsukasa et al. 2006; O'Neill et al. 2018; Ogihara et al. 2007; Pontzer et al. 2014; Sockol et al. 2007; Thompson et al. 2021; Vereecke et al. 2006). In the literature, two main approaches can be found, the observational and experimental approaches. The observational approach concerns the studies in which the variables are not controlled. It records the behaviour of an animal when and where it happens and thus presents inherent limitations. The experimental approach aims at controlling important independent variables that can influence the dependent variable under study (e.g. bipedal kinematics, kinetics, EMG) so that the researchers can directly evaluate causes and effects (see figure 2 for examples). The experimental approach can thus open new perspectives and provide important insights into key aspects that remain difficult to study in free-ranging or uncontrolled conditions. For instance, the diversity of foot postures during bipedal walking remains poorly documented in non-human primates (but see Berillon et al. 2010; Holowka et al. 2017; Vereecke et al. 2003; Vereecke et al. 2005; Vereecke & Aerts 2008), as well as how these are affected by substrate variation. The movements of the pelvis, the lower back, the forelimbs, including hand positioning and use, are also poorly documented during bipedalism. Recent experimental studies have started to explore the movements of the trunk during bipedal walking and have revealed more flexibility than was initially predicted (Kinoshita et al. 2021; O'Neill et al. 2018; Thompson et al. 2015; Thompson et al. 2018). The study of the transitions from another locomotor mode to bipedal walking is also an area of research where there is a lack of experimental data (but see Mori et al. 2006; Nakajima et al. 2001). Studying the biomechanics of bipedalism with an experimental approach in non-human primates can allow accurately exploration of these aspects and therefore help us to better understand the evolution of the bipedal locomotor mode in primates, including hominins.

5However, compared to the experimental biomechanical protocols applied in human locomotion, conducting an experiment on non-human primate locomotion represents a big challenge as it requires bringing the animal in close contact with the researchers and with fragile and expensive measurement equipment. In this context, using positive reinforcement techniques, as part of the experimental study procedure, can offer the possibility of conducting unique research protocols. Working with a cooperative animal can approach the standards of human-based studies and also direct comparisons of the data collected in humans with those collected in non-human primates. It also ensures an optimal level of the Refinement component of the "3Rs" rule (Russell & Burch, 1959).

Figure 2

Figure 2

The three illustrations were extracted from previously published scientific papers. (A) shows skeletal postures of a chimpanzee walking bipedally obtained from cineradiography and is after figure 1 in Jenkins (1972), (B) shows a Japanese macaque with his trainer in an experimental chamber and the illustration is after figure 2 in Nakatsukasa et al. (2004) and (C) shows a chimpanzee walking bipedally on a treadmill as part of UC Davis anthropologist Michael Sockol's research (see Sockol et al. 2007) ©Cary Wolinsky.

3 The use of positive reinforcement techniques to study bipedal walking in baboons

6Movement performance is strongly influenced by several variables, such as the speed of progression and the direction of movement (e.g. Alexander, 1976; Alexander & Jayes, 1983). It is possible to apply a post-hoc control of these variables, but this reduces the amount of data available for the analyses and the sampling effort needs to be enormously increased to compile enough exploitable data. Based on our experience of both, experimental and behavioural studies in olive baboons (e.g. Berillon et al. 2010; Anvari et al. 2014; Druelle et al. 2017), our team aimed at setting up an experiment on this species that makes possible to control, a priori, these variables and optimize repeatability. During the last decade, our team has implemented different training protocols based on positive reinforcement in the context of the study of locomotion in baboons, including bipedal walking. Positive reinforcement occurs when a desirable event, or stimulus, is presented because of a behaviour, hence the likelihood that this behaviour would happen again in similar conditions increases. Our goal was thus to accommodate the baboons to walk bipedally in an instrumented environment, including surface electrodes for the study of muscular activity and a treadmill. The use of such a device allowed us to control speed and direction of movement and at the same time to collect large datasets in terms of walking cycles, thus optimizing repeatability.

7Here, we present the main protocol that we developed and implemented at the Primatology Station of the CNRS (UAR 846) to study bipedal and quadrupedal locomotion in olive baboons, Papio anubis. This protocol allows to reach the accuracy of the experimental protocols applied in humans (e.g. Berillon et al. 2013; Druelle et al. 2021). Our aim is to document the way we trained the animals using positive reinforcement techniques, as well as the amount of training necessary for baboons (and potentially for other non-human primate models) to walk bipedally and quadrupedally on a treadmill. Finally, we highlight the possibilities opened up by such an approach for the study of bipedalism in non-human primates in general. Note that according to the current international ethical regulations, the present protocol including anaesthesia of the animals cannot be implemented in apes (see the Directive 2010/63/EU of the European Parliament and of the council of 22 September 2010 on the protection of animals used for scientific purposes ; https://eur-lex.europa.eu/​legal-content/​EN/​TXT/​HTML/​?uri=CELEX:32010L0063). The procedure described here on baboons was evaluated by ethical committees on animal experimentation and approved by the French Ministry of Higher Education and Research (Project 68-19112012, CEEA-14 Marseille, and Project APAFIS#16621-2018090509386918 v2, ethical committee n°071).

8Different learning techniques, and not only positive reinforcement, were used here to train the animals to cooperate during experiments. Positive reinforcement learning paradigm, i.e., rewarding the animal when performing the desired behaviour, and systematic desensitization were the main techniques used here (Prescott & Buchanan-Smith, 2016; Schapiro et al. 2003). No coercion was used, and mistakes were ignored, not punished. The animal was always able to choose whether it was willing to participate in the training program or not (for a review of all these techniques, see Pryor, 2019). As a result, we have worked with the voluntary cooperation of the animals, thus ensuring the highest level of the Refinement component of the "3Rs" rule (Russell & Burch, 1959).

3.1 Selection of the animals

9Selection of the animals for the experiments was done using a very simple "boldness test". The trainers offered treats by hand to several naive individuals in a social group. The first two females that took the food reward from the trainers’ hand were selected as study animals. A natural trend to interact with humans, as well as curious and greedy animals, represented the best option to start with. The four olive baboons that were included in the study (2 in 2013 and 2 in 2019) were housed at the Primatology Station of the CNRS (Rousset-sur-Arc, France). They spent their first year of life with their mother and within their social group. There was no direct contact with humans during this period. After the animals were weaned, they were moved from their social group and put together in a large indoor cage.

3.2 The food rewards

10Several food rewards were used during the training sessions. These were fresh fruits, dried pasta and dried fruits. If available, fresh fruits (representing a healthier reward) were always preferred and attempts were made to avoid the use of sweet items. The food items were cut into small pieces to keep the animals motivated as much as possible and to avoid a rapid satiety. We rapidly noticed that each individual had its own treat preferences. As treat value increases with scarcity, we adjusted as much as possible the different types of rewards to keep animals motivated. To facilitate the learning process, we used a clicker as a "bridge" between the command and the correct behaviour, and as a secondary reinforcer (Feng et al. 2016).

3.3 Duration of the training sessions

11The duration of the training sessions varied from 15 to 30 minutes per individual and per day. Animals were trained from Monday to Friday. The end of a session was determined by the motivation of the animal, i.e., a reduction in the performance of the animal, or the declining interest in the training and in the food reward. If an animal showed an aggressive behaviour toward a congener or the trainers, the training session was ended immediately.

3.4 The shaping procedure

12The training process of the animals was organized step-by-step. The process of reinforcing successively and gradually approximations to a desired behaviour is called "shaping". Before the start of the shaping process, the expected behaviour, i.e., to walk, on demand, quadrupedally and bipedally on a treadmill in a specific experimental setup, was split into different phases of increasing complexity. For example, entering the experimental setup required the animals to be transferred from their enclosure to the experimental room. To do so, we first trained the animals to present their necks and collars (1), second to accept a leash (2), and third to walk side by side with the trainer (3).

13During the first stages of the shaping process, we reinforced any response or behaviour that was close to the desired behaviour (e.g. presenting the neck to leashing). Once this behaviour was properly learned, we stopped reinforcing it and started to reinforce the response close to the next desired behaviour (e.g. to stay still when clipping the leash).

14Below, we present the main steps of the shaping process:

  1. Systematic desensitization to the trainer - This desensitization, or counterconditioning (Schapiro et al. 2003), consists of a gradual exposure to an aversive stimulus (i.e. the close presence to the trainer) coupled with a primary reinforcer (i.e. treats). The aim of this technique is to reduce anxiety, stress, and avoidance by gradually exposing the individual to the source of their discomfort in a thoughtfully planned way. It promotes habituation to the close proximity of the trainer and generates a great amount of positive interactions. This first training period was carried out in an indoor cage, thus allowing the trainer to come inside, in close contact, with the animals.

  2. “Charging the clicker” - The individuals were trained to associate the sound of the clicker to a food reward, i.e. the trainer clicked and then rewarded the animal systematically. Once the animals learn this contingency, the clicker can then be used as a "bridge" and a secondary reinforcer to precisely point the behaviour to reinforce (Feng et al. 2016; Williams et al. 2004).

  3. Training some foundation behaviours - We trained the animals to give the right and left hands and the feet on demand. The teaching of these very simple four foundation behaviours have several goals. First, these interactions allow us to build up a relationship of "trust" with the animals. This enables deepening the desensitization process and accelerating the shaping process. Second, it facilitates the proper understanding of the “order-behaviour-click-reward” contingency process, thus facilitating the learning of future behaviours.

  4. Parking training - We trained the animals to stand still and wait the order from the trainer before behaving. We teach this by ignoring behavioural responses that are not preceded by an order.

  5. Collar presentation - We trained the baboons to present their neck and their collar with the aim of facilitating the leashing action.

  6. Systematic desensitization to the carabiner and the leash – First, the animals were desensitized to be clipped with the carabiner. Second, the animals were desensitized to be clipped with the carabiner attached to the leash.

  7. Training to go outside of the enclosure - Once the animals were trained to be leashed, we proposed them to go out of their enclosure. This process was performed step by step by luring the animals outside their cage. During this desensitization process, the animals could get back inside their enclosure whenever they wanted.

  8. Training to walk nearby the trainer - Once the animal felt comfortable outside the cage the trainer started to walk nearby the animal until it was able to "synchronize" its walk with the speed of the trainer walk.

  9. Training to walk bipedally - We did not systematically train the animals to walk bipedally, but instead to stand up on two legs for reaching the treat. Once in this position, we were keeping the treat far out of their reach to facilitate the execution of two or three complete gait cycles.

  10. Desensitisation to the setup - The final training phase was the desensitization of the animals to the experimental setup, i.e., the enclosure where the experiments would be conducted. The animals were taken several times with the leash to this new enclosure where the treadmill was placed. In this environment, they could be released and fed on the treadmill in movement.

  11. Training to keep walking - Once the animals accepted interaction with the trainer while walking quadrupedally on the treadmill, it was quite easy to make the animals take the treat in a bipedal posture. Our final goal was to maximize the number of bipedal gait cycles between the quadrupedal-bipedal transition phase and retrieval of the treat. We introduced the order to stand up and we increased systematically the delay between the "click" and the treat. Walking bipedally on the treadmill at different speeds was achieved in few sessions (<20) after being in contact with the device.

TABLE 1

TABLE 1

Training schedule for the two individuals trained in 2019 using positive reinforcement technique

15The aforementioned protocol was applied to two female individuals in 2013 (trained by PMV) and two others in 2019 (trained by FD). Table 1 and figure 3 show the general work flow of this protocol, from birth of the animals to the first experiments. As far as the individuals trained in 2019 are concerned, one individual made her first bipedal steps during the second session in contact with the treadmill device, and the first bipedal behaviour occurred at the 4th session. We have estimated at 75 minutes the time this female spent walking on the treadmill before the experiments (15 sessions of 5 minutes in average). The second female needed 12 sessions to accept walking on the treadmill. We have estimated that she spent 40 minutes on the treadmill before the start of the experiments. In total, after 23 weeks of training, including 125 sessions (for both individuals), the baboons were properly trained, and the experiments could start. The first session of data collection took place the 24th of October 2019 and allowed us to collect 3D kinematics of bipedal walking. The second session of data collection took place on the 28th and 29th of November and allowed us to collect data on the muscular activity during bipedal and quadrupedal walking using surface probes. No specific training was done for the instrumentation of the animals. Before the EMG experiments, the individuals were anesthetized to allow us to locally shave, clean and degrease the skin and to ensure accurate electrode placement (see Druelle et al. 2021). In summary, accurate 3D kinematics and EMG data of the hindlimb and back muscles were collected in these young baboons, while controlling the direction and speed of the animals using a treadmill device.

Figure 3

Figure 3

Workflow of the training process using Positive Reinforcement Techniques (PRT), from birth to the first experimental work including kinematics and EMG on bipedal walking. The pictures on the left-hand side show the early life of the baboons living in their social group at the primatology station of the CNRS. The pictures in the middle are examples of the variability of postures adopted by a young female olive baboon, Ophélie (Id1), when moving on a treadmill during a training session of ~5 minutes. The picture on the right-hand side shows a baboon equipped with surface electrodes walking bipedally on a treadmill during a session of data collection.

4 Conclusion and perspectives

16In the present report, we have shown that a few minutes, spread over a relatively small amount of training sessions, are needed to make a pronograde non-human primate (the olive baboon) accept walking bipedally on a treadmill at different speeds. The treadmill is a very relevant device to use for collecting accurate and reproducible biomechanical data of primate locomotion. While Tuttle et al. (1979) noted already in 1979 that the methods of recording and analysing data in animal experimentation differ between studies and may hinder the interpretation of the dissimilarities between the results to functional aspects, this observation appears to remain true today. Conducting experimental studies in which the training is used and documented may already yield valuable insight into future studies about primate locomotion. The unique nature and the accuracy of the data collected in these setups make it highly relevant and valuable for our understanding of bipedal locomotion in non-human primates and it helps reach the standards of the study of human movement. Based on these biomechanical data and the fossil record, new modelling approaches can now propose simulations of extinct species (e.g. DeSilva et al. 2013; Nicolas et al. 2007). Going further into our understanding of the bipedal behaviour in our closest relatives also requires collecting accurate 3D kinematics (Demes, 2011; Kinoshita et al. 2021; O'Neill et al. 2018; Thompson et al. 2021; Vereecke et al. 2006) and to test how their bipedal walking pattern is likely to be affected by the speed of progression and variations in the substrate. In this context, appropriate refinement procedures such as the one presented here can significantly facilitate the work with these animals (see also other examples; Foster et al. 2014).

17In addition, positive reinforcement methods can allow electromyographic studies. These can also provide important insights into primate locomotion, by providing unique perspectives for our understanding of human bipedal evolution (Higurashi et al. 2019; Stern & Susman, 1981). However, setting such experiments is dramatically challenging due to constraints related to legislation (country-related), technical material and behaviour of the animal (e.g. stress management). For instance, surgical/insertion procedures are commonly needed in order to insert the electrodes into the focal muscles (e.g. Boyer et al. 2007; Courtine et al. 2005; Higurashi et al. 2019; Stern & Susman, 1981). This invasive procedure could be a source of veterinary problems, disturb the normal walking patterns and bring inherent replicability problems. With regard to surface electrodes, low intra-operator repeatability and inter-operator reproducibility have been emphasised in humans for the collection of high-quality EMG signals for gait analysis (see Agostini et al. 2020, for a review). As a consequence, this field certainly suffers from a great diversity of methodological approaches and varied experimental conditions, which make the data heterogeneous and difficult to compare quantitatively. As also pointed out in humans (Agostini et al. 2020), there is a clear lack of normative data for what concerns the general muscular activity pattern during walking in non-human primates. For instance, muscle activation is obviously modulated by the speed of locomotion (Courtine et al. 2005), yet, this information has been regularly missing in the primate literature about muscle activity, and more generally in kinematics and kinetic studies. The use of trained individuals to walk at constant speed using a treadmill device clearly solve this issue.

18To conclude, non-human primates have been increasingly studied in their natural environment, as well as in captive settings, for various purposes within the fields of (palaeo)anthropology, neuroscience, ethology, psychology, evolutionary biology, etc. Here, we have focused on the study of locomotion, and more specifically on the experimental study of bipedal locomotion in the context of evolutionary biology and palaeoanthropology. There is no doubt that studying bipedal behaviour in non-human primates can help us to better understand the evolutionary transition toward habitual bipedalism in hominins. Nevertheless, a full understanding of the acquisition of a habitual bipedal gait requires the study of bipedal walking in a broad range of non-human primates at various and finer levels. In our opinion, studies including cooperative animals that can freely move and accept wearing specific material is one of the most valuable experimental tools for filling this gap of knowledge over the next decades.

Acknowledgements

19We are very grateful to Romain Lacoste, former director of the Primatology Station of the CNRS, and Gilles Berillon, Principal Investigator of the project (UMR 7194 CNRS-MNHN-UPVD) and co-responsible of the Technical Platform "Motion Analysis of Primates", who both initiated these experiments at the CNRS Primatology Station in 2012. We are very grateful to Christophe Arnoult, the current director of the Primatology Station of the CNRS, for his support. We also thank Brigitte Rimbaud for her participation in the training protocol conducted on the first two female baboons in 2013. We thank Martin Pickford who revised the English of the manuscript and Brigitte Senut who carefully checked the last version of the manuscript. We thank Evie Vereecke for her constructive comments on the previous version of the manuscript and we are grateful to an anonymous referee for the detailed comments. This project has been successively funded by the CNRS International Pluridisciplinary Network "Humans and Non-human Primates", by the CNRS International Research Network n°GDRI0870 "Bipedal Equilibrium" and by the HoBiS (Hominine BipedalismS) ANR Project n°ANR-18-CE27-0010-01 (G. Berillon Dir.).

Conflict of Interest

20The authors declare that they have no competing interests.

Haut de page

Bibliographie

Aerts P, Van Damme R, Van Elsacker L, Duchene V. 2000. Spatio-temporal gait characteristics of the hind-limb cycles during voluntary bipedal and quadrupedal walking in bonobos (Pan paniscus). American journal of physical anthropology 111: 503-517.

Alexander RM. 1976. Estimates of speeds of dinosaurs. Nature 261(5556): 129-130.

Alexander RM. 2004. Bipedal animals, and their differences from humans. Journal of Anatomy 204(5): 321-330.

Alexander RM, Jayes AS. 1983. A dynamic similarity hypothesis for the gaits of quadrupedal mammals. Journal of Zoology 201(1): 135-152.

Anvari Z, Berillon G, Asgari Khaneghah A, Grimaud-Herve D, Moulin V, Nicolas G. 2014. Kinematics and spatiotemporal parameters of infant-carrying in olive baboons. American Journal of Physical Anthropology 155(3): 392-404.

Agostini V, Ghislieri M, Rosati S, Balestra G, Knaflitz M. 2020. Surface Electromyography Applied to Gait Analysis: How to Improve Its Impact in Clinics? Frontiers in Neurology 11: 994.

Berillon G, Daver G, D’Août K, et al. 2010. Bipedal versus Quadrupedal Hind Limb and Foot Kinematics in a Captive Sample of Papio anubis: Setup and Preliminary Results. International Journal of Primatology 31(2): 159-180.

Berillon G, Molina-Vila P, Lacoste R, et al. 2013. Biomechanics and Control of Walking in Olive Baboons (Papio anubis): New Perspectives from Trained and Instrumented Animals. Folia Primatologica 84: 249.

Boyer DM, Patel BA, Larson SG, Stern Jr JT. 2007. Telemetered electromyography of peroneus longus in Varecia variegata and Eulemur rubriventer: implications for the functional significance of a large peroneal process. Journal of Human Evolution 53(2): 119-134.

Charles JP, Grant B, D'Août K, Bates KT. 2021. Foot anatomy, walking energetics, and the evolution of human bipedalism. Journal of Human Evolution 156: 103014.

Courtine G, Roy RR, Hodgson J, et al. 2005. Kinematic and EMG determinants in quadrupedal locomotion of a non-human primate (Rhesus). Journal of Neurophysiology 93(6): 3127-3145.

Crompton R, Vereecke E, Thorpe S. 2008. Locomotion and posture from the common hominoid ancestor to fully modern hominins, with special reference to the last common panin/hominin ancestor. Journal of Anatomy 212(4): 501-543.

D'Août K, Vereecke E, Schoonaert K, De Clercq D, Van Elsacker L, Aerts P. 2004. Locomotion in bonobos (Pan paniscus): differences and similarities between bipedal and quadrupedal terrestrial walking, and a comparison with other locomotor modes. Journal of Anatomy 204(5): 353-361.

Demes B. 2011. Three-dimensional kinematics of capuchin monkey bipedalism. American Journal of Physical Anthropology 145(1): 147-155.

DeSilva JM, Holt KG, Churchill SE, Carlson KJ, Walker CS, Zipfel B, Berger LR. 2013. The lower limb and mechanics of walking in Australopithecus sediba. Science 340(6129):1232999.

Druelle F, Supiot A, Meulemans S, et al. 2021. The quadrupedal walking gait of the olive baboon, Papio anubis: an exploratory study integrating kinematics and EMG. Journal of Experimental Biology 224(14): jeb242587.

Elftman H. 1944. The bipedal walking of the chimpanzee. Journal of Mammalogy 25(1): 67-71.

Elftman H, Manter J. 1935. Chimpanzee and human feet in bipedal walking. American Journal of Physical Anthropology 20(1): 69-79.

Esrafilian A, Stenroth L, Mononen M, Tanska P, Avela J, Korhonen R. 2020. EMG-assisted muscle force driven finite element model of the knee joint with fibril-reinforced poroelastic cartilages and menisci. Scientific Reports 10(1): 1-16.

Feng LC, Howell TJ, Bennett PC. 2016. How clicker training works: Comparing Reinforcing, Marking, and Bridging Hypotheses. Applied Animal Behaviour Science 181: 34-40.

Foster JD, Nuyujukian P, Freifeld O, et al. 2014. A freely-moving monkey treadmill model. Journal of Neural Engineering 11(4): 046020.

Higurashi Y, Maier MA, Nakajima K, et al. 2019. Locomotor kinematics and EMG activity during quadrupedal versus bipedal gait in the Japanese macaque. Journal of Neurophysiology 122(1): 398-412.

Hirasaki E, Ogihara N, Hamada Y, Kumakura H, Nakatsukasa M. 2004. Do highly trained monkeys walk like humans? A kinematic study of bipedal locomotion in bipedally trained Japanese macaques. Journal of Human Evolution 46(6): 739-750.

Hirasaki E, Ogihara N, Nakatsukasa M. 2006. Primates trained for bipedal locomotion as a model for studying the evolution of bipedal locomotion. In H Ishida, R Tuttle, M Pickford, N Ogihara & M Nakatsukasa (Eds.), Human Origins and Environmental Backgrounds (pp. 149-155.). Boston, Springer.

Holowka NB, O'Neill MC, Thompson NE, Demes B. 2017. Chimpanzee and human midfoot motion during bipedal walking and the evolution of the longitudinal arch of the foot. Journal of Human Evolution 104: 23-31.

Ishida H, Kimura T, Okada M. 1974. Patterns of bipedal walking in anthropoid primates. In Proceedings of the 5th Congress of the International Primatological Society (pp. 287-301).

Jenkins FA. 1972. Chimpanzee bipedalism: cineradiographic analysis and implications for the evolution of gait. Science 178(4063): 877-879.

Kimura T, Okada M, Ishida H. 1979. Kinesiological characteristics of primate walking: its significance in human walking. In ME Morbeck, H Preuschoft & N Gomberg (Eds.), Environment, Behavior, and Morphology: Dynamic Interactions in Primates (pp. 297-311). New York, Gustav Fisher.

Kinoshita Y, Goto R, Nakano Y, Hirasaki E. 2021. A comparison of axial trunk rotation during bipedal walking between humans and Japanese macaques. American Journal of Physical Anthropology 174(1): 66-75.

Kirtley C. 2006. Clinical Gait Analysis: Theory and Practice. Elsevier Health Sciences.

Mori F, Nakajima K, Tachibana A, Mori S. 2006. Obstacle clearance and prevention from falling in the bipedally walking Japanese monkey, Macaca fuscata. Age and ageing 35(suppl_2): ii19-ii23.

Nakajima K, Mori F, Takasu C, Tachibana A, Okumura T, Mori M, Mori S. 2001. Integration of Upright Posture and Bipedal Locomotion in Non-Human Primates. In: R Dengler & AR Kossev (Eds.), Sensorimotor Control (pp. 95-102). IOS Press.

Nakatsukasa M, Hirasaki E, Ogihara N. 2006. Energy expenditure of bipedal walking is higher than that of quadrupedal walking in Japanese macaques. American Journal of Physical Anthropology 131(1) :33-37.

Nakatsukasa M, Ogihara N, Hamada Y, Goto Y, Yamada M, Hirakawa T, Hirasaki E. 2004. Energetic costs of bipedal and quadrupedal walking in Japanese macaques. American Journal of Physical Anthropology 124(3): 248-256.

Nicolas G, Multon F, Berillon G, Marchal F. 2007. From bone to plausible bipedal locomotion using inverse kinematics. Journal of Biomechanics 40(5): 1048-1057.

Ogihara N, Hirasaki E, Kumakura H, Nakatsukasa M. 2007. Ground-reaction-force profiles of bipedal walking in bipedally trained Japanese monkeys. Journal of Human Evolution 53(3): 302-308.

O'Neill MC, Demes B, Thompson NE, Umberger BR. 2018. Three-dimensional kinematics and the origin of the hominin walking stride. Journal of The Royal Society Interface 15(145): 20180205.

Pontzer H. 2017. Economy and endurance in human evolution. Current Biology 27(12): R613-R621.

Pontzer H, Raichlen DA, Rodman PS. 2014. Bipedal and quadrupedal locomotion in chimpanzees. Journal of Human Evolution 66: 64-82.

Prescott MJ, Buchanan-Smith HM. 2016. Training Nonhuman Primates Using Positive Reinforcement Techniques: A Special Issue of the Journal of Applied Animal Welfare Science: Psychology Press.

Prost JH. 1967. Bipedalism of man and gibbon compared using estimates of joint motion. American Journal of Physical Anthropology 26(2): 135-148.

Pryor K. 2019. Don't Shoot the Dog: The Art of Teaching and Training. Simon & Schuster.

Russell WMS, Burch RL. 1959. The Principles of Humane Experimental Technique. Methuen.

Schapiro SJ, Bloomsmith MA, Laule GE. 2003. Positive reinforcement training as a technique to alter nonhuman primate behavior: quantitative assessments of effectiveness. Journal of Applied Animal Welfare Science 6(3): 175-187.

Sockol MD, Raichlen DA, Pontzer H. 2007. Chimpanzee locomotor energetics and the origin of human bipedalism. Proceedings of the National Academy of Sciences 104(30): 12265-12269.

Stern JT, Susman RL. 1981. Electromyography of the gluteal muscles in Hylobates, Pongo, and Pan: Implications for the evolution of hominid bipedality. American Journal of Physical Anthropology 55(2): 153-166.

Taylor CR, Rowntree VJ. 1973. Running on Two or on Four Legs: Which Consumes More Energy? Science 179(4069): 186-187.

Thompson NE, Demes B, O'Neill MC, Holowka NB, Larson SG. 2015. Surprising trunk rotational capabilities in chimpanzees and implications for bipedal walking proficiency in early hominins. Nature Communications 6.

Thompson NE, O'Neill MC, Holowka NB, Demes B. 2018. Step width and frontal plane trunk motion in bipedal chimpanzee and human walking. Journal of Human Evolution 125: 27-37.

Thompson NE, Rubinstein D, Parrella-O'Donnell W, Brett MA, Demes B, Larson SG, O'Neill MC. 2021. The loss of the 'pelvic step' in human evolution. Journal of Experimental Biology 224(16): jeb240440.

Tuttle RH, Basmajian JV, Ishida H. 1979. Activities of pongid thigh muscles during bipedal behavior. American Journal of Physical Anthropology 50(1): 123-135.

Vereecke E, D'Août K, De Clercq D, Van Elsacker L, Aerts P. 2003. Dynamic plantar pressure distribution during terrestrial locomotion of bonobos (Pan paniscus). American Journal of Physical Anthropology: The Official Publication of the American Association of Physical Anthropologists 120(4): 373-383.

Vereecke EE, Aerts P. 2008. The mechanics of the gibbon foot and its potential for elastic energy storage during bipedalism. Journal of Experimental Biology 211(23): 3661-3670.

Vereecke EE, D'Août K, Aerts P. 2006. Speed modulation in hylobatid bipedalism: A kinematic analysis. Journal of Human Evolution 51(5): 513-526.

Vereecke E, D'Août K, Van Elsacker L, De Clercq D, Aerts P. 2005. Functional analysis of the gibbon foot during terrestrial bipedal walking: Plantar pressure distributions and three-dimensional ground reaction forces. American Journal of Physical Anthropology 128(3): 659-669.

Williams JL, Friend TH, Nevill CH, Archer G. 2004. The efficacy of a secondary reinforcer (clicker) during acquisition and extinction of an operant task in horses. Applied Animal Behaviour Science 88(3): 331-341.

Winter DA. 2009. Biomechanics and Motor Control of Human Movement. John Wiley & Sons.

Wu AR, Simpson CS, van Asseldonk EH, van der Kooij H, Ijspeert AJ. 2019. Mechanics of very slow human walking. Scientific Reports 9(1): 1-10.

Haut de page

Document annexe

  • Version française (application/pdf – 626k)

    Ce document est une traduction en français de l'article original rédigé en anglais. Cette traduction a été réalisée par le premier auteur de l'article, FD.

Haut de page

Table des illustrations

Titre Figure 1
Légende Illustrations showing a human individual equipped with a motion capture system with EMG to study knee joint loading and a baboon standing bipedally in a flexed posture. The illustration of the human individual was extracted from Esrafilian et al. (2020). The illustration on the right-hand side was taken by FD and shows a baboon raised in captivity at the primatology station of the CNRS.
URL http://journals.openedition.org/primatologie/docannexe/image/11455/img-1.jpg
Fichier image/jpeg, 330k
Titre Figure 2
Légende The three illustrations were extracted from previously published scientific papers. (A) shows skeletal postures of a chimpanzee walking bipedally obtained from cineradiography and is after figure 1 in Jenkins (1972), (B) shows a Japanese macaque with his trainer in an experimental chamber and the illustration is after figure 2 in Nakatsukasa et al. (2004) and (C) shows a chimpanzee walking bipedally on a treadmill as part of UC Davis anthropologist Michael Sockol's research (see Sockol et al. 2007) ©Cary Wolinsky.
URL http://journals.openedition.org/primatologie/docannexe/image/11455/img-2.jpg
Fichier image/jpeg, 158k
Titre TABLE 1
Légende Training schedule for the two individuals trained in 2019 using positive reinforcement technique
URL http://journals.openedition.org/primatologie/docannexe/image/11455/img-3.jpg
Fichier image/jpeg, 225k
Titre Figure 3
Légende Workflow of the training process using Positive Reinforcement Techniques (PRT), from birth to the first experimental work including kinematics and EMG on bipedal walking. The pictures on the left-hand side show the early life of the baboons living in their social group at the primatology station of the CNRS. The pictures in the middle are examples of the variability of postures adopted by a young female olive baboon, Ophélie (Id1), when moving on a treadmill during a training session of ~5 minutes. The picture on the right-hand side shows a baboon equipped with surface electrodes walking bipedally on a treadmill during a session of data collection.
URL http://journals.openedition.org/primatologie/docannexe/image/11455/img-4.jpg
Fichier image/jpeg, 352k
Haut de page

Pour citer cet article

Référence électronique

François Druelle et Pablo Molina-Vila, « A baboon walking on a treadmill: the use of positive reinforcement techniques to study bipedal walking in non-human primates »Revue de primatologie [En ligne], 12 | 2021, mis en ligne le 10 mars 2022, consulté le 24 mars 2023. URL : http://journals.openedition.org/primatologie/11455 ; DOI : https://doi.org/10.4000/primatologie.11455

Haut de page

Auteurs

François Druelle

UMR 7194 (Histoire Naturelle de l'Homme Préhistorique), CNRS-Muséum National d'Histoire Naturelle-UPVD, Musée de l'Homme, 17 Place du Trocadéro, 75116 Paris, France
Corresponding author: francois.druelle@mnhn.fr

Articles du même auteur

Pablo Molina-Vila

UAR 846 Station de primatologie du CNRS, Routes des 4 tours, 13790 Rousset-sur-Arc, France
pablo.molinavila@primato.cnrs.fr

Haut de page

Droits d’auteur

CC-BY-NC-ND-4.0

Creative Commons - Attribution - Pas d'Utilisation Commerciale - Pas de Modification 4.0 International - CC BY-NC-ND 4.0

https://creativecommons.org/licenses/by-nc-nd/4.0/

Haut de page
Rechercher dans OpenEdition Search

Vous allez être redirigé vers OpenEdition Search