While bipedal locomotion is seen as a major functional change during the course of hominin evolution, our understanding of the adjustments that occurred in the motor control to make bipedal walking possible for long periods of time remains very speculative (e.g., Stern and Susman, 1981; Vilensky, 1987; Dominici et al., 2011). Based on the intriguing association of anatomical traits pointing toward bipedal behavior, recent paleontological discoveries (e.g., Orrorin tugenensis, Sahelanthropus tchadensis) allow addressing whether bipedalism might have been habitually used very early in the hominin lineage (e.g., Senut et al., 2001; White et al., 2015; Daver et al., 2022), and also possibly before the emergence of hominins (in a few specific Miocene hominoids, i.e., 23–6 Ma, such as in Oreopithecus bambolii and Danuvius guggenmosi; Rook et al., 1999; Böhme et al., 2019). In early hominins, bipedalism might have been habitually used in combination with other locomotor modes, including (arboreal) quadrupedal behaviors (Rose, 1991; Senut, 2007; Green and Alemseged, 2012; DeSilva et al., 2018; Almécija et al., 2021; Daver et al., 2022; Meyer et al., 2023; Stamos and Alemseged, 2023; Urciuoli and Alba, 2023).

Catarrhines have a ‘quadrupedal bauplan’ generally adapted to arboreal locomotion (e.g., Cartmill, 1972; Rose, 1973; Cartmill et al., 2002; Schmitt et al., 2006; Granatosky et al., 2017; Cartmill et al., 2020). They can cope with important balance and maneuverability requirements, and they may rely on increased and continuous sensory feedback compared to other mammals (Eidelberg et al., 1981). Locomotor control has been hypothesized to be organized differently in these species compared to other mammals (Eidelberg et al., 1981; Vilensky, 1987; Courtine et al., 2005; Larson and Stern, 2007). One can also consider that non-human primates are freed, in some respects, from the (anatomical) constraints related to strict quadrupedal locomotion and coordination as they develop complex locomotor repertoires (Hunt et al., 1996). Catarrhines are also able to stand and occasionally walk bipedally (e.g., baboon: Rose, 1976; Druelle et al., 2017; chimpanzee: Stanford, 2006; Carvalho et al., 2012; Pernel et al., 2021; langur: Workmann and Schmitt, 2011; colobe: Morbeck, 1977; Gebo and Chapman, 1995; macaques: Wells and Turnquist, 2001; orangutans: Thorpe et al., 2007; and for a review, see Druelle and Berillon, 2014) despite anatomies that do not bear the skeletal traits usually understood as bipedal locomotor adaptations in hominins. Their anatomy allows bipedal walking in the so-called ‘bent-hip, bent-knee’ posture, which acknowledges that they do not use extended limb postures as observed in humans (Alexander, 2004; Hirasaki et al., 2004; Ogihara et al., 2010; Demes and O'Neill, 2013; Pontzer et al., 2014; Demes et al., 2015; Thompson et al., 2015; O'Neill et al., 2018; Blickhan et al., 2021; Thompson et al., 2021). As recently shown in a comparative study in captivity, extant catarrhines (i.e., bonobos, chimpanzees, gorillas, orangutans, hylobatids, siamangs, baboons, and mandrills in this study) are using bipedal walking for very short bouts during their daily activities (Rosen et al., 2022; see also Rose, 1976; Hunt, 1994; Stanford, 2006; Thorpe et al., 2007; Druelle et al., 2016), but the evolutionary transition toward habitual bipedalism obviously required a stronger involvement into this mode. As a result, such a widespread behavior observed in many extant species let us suggest that it was also the case in Miocene hominoids. The most parsimonious hypothesis remains that they were already using bipedalism, at least occasionally, which involves motor control mechanisms similar to extant non-human primate species.

Terrestrial bipedal walking requires the central nervous system to modulate and coordinate the contraction of many muscles and greater balance adjustments are needed compared to quadrupedal walking. In a bipedal posture, the body center of mass needs to be balanced on two legs and lies above the hip joints within a small support polygon; in a quadrupedal posture, the body center of mass is positioned between four legs and anterior to the hip joints in a large support polygon (Kimura, 1996; Raichlen et al., 2009; Druelle et al., 2019). Bipedal walking in non-human primates may thus require to achieve a different muscle coordination toward higher muscle coactivation than during quadrupedal walking (Higurashi et al., 2019). In humans, a modular organization of the neuromuscular control, the so-called ‘muscle synergies’, have been suggested (Grillner, 1985; Ivanenko et al., 2004; Dominici et al., 2011; Torricelli et al., 2016) that would make this locomotor task simplified at the level of the motor control strategy (Dominici et al., 2011; Lacquaniti et al., 2012). Each synergy defines a group of coactivated muscles that are expected to work together as a single functional unit. Based on the analysis of muscle synergies, the existence of four basic activation patterns have been shown to be shared, in some respects, in rats, cats, macaques, guineafowl, and humans during walking (Dominici et al., 2011). This analysis does not contradict the potential specificities within primate neural networks but highlights the conservation of a common ancestral neural network for the execution of stepping. The application of this approach in various species and in different tasks has revealed that complex muscle patterns are commonly reconstructed with only a few muscle synergies. This approach has also been widely used for the assessment and rehabilitation of neuromotor diseases in humans (Safavynia et al., 2011; Taborri et al., 2018). Understanding the affinities between locomotor modes in primates can significantly contribute to the development of evolutionary scenarios for the transition toward locomotor specializations (e.g., Fleagle et al., 1981; Stern and Susman, 1981; Aerts et al., 2000; Berillon et al., 2011; Granatosky et al., 2016; Granatosky and Schmitt, 2019; Aerts et al., 2023). For instance, it can help to understand the link between quadrupedal and bipedal locomotion in primates in general (see Vangor and Wells, 1983; Vilensky, 1987; Shapiro and Jungers, 1994; Balter and Zehr, 2007; Zehr et al., 2009; Higurashi et al., 2019; Aerts et al., 2023) and to explore, in a comparative and evolutionary framework, what has to be resolved to specialize for bipedal locomotion (e.g., hip joint stabilization, propulsion generation, controlling the trunk position, controlling foot clearance). Therefore, understanding the motor affinities between locomotor modes in primates is likely to provide important insights into the (evolutionary) process of transitioning from a locomotor repertoire based on quadrupedalism to a repertoire based on bipedalism (e.g., Taylor and Rowntree, 1973; Foster et al., 2013; Kozma et al., 2018; Raichlen and Pontzer, 2021).

Here, we study motor control strategies through the muscle synergy theory of a quadrupedal primate, the olive baboon, Papio anubis, when walking quadrupedally and bipedally on the ground in comparison to those of humans. Undoubtedly, the morphology of baboons is specialized for quadrupedal walking, and their musculoskeletal system differs significantly from what is expected and observed in early hominins or Miocene apes. However, despite its specificities (see D’Août et al., 2014), this comparative model can offer valuable insights into how a quadrupedal primate naturally addresses the challenge of walking bipedally during its daily activities (e.g., Rose, 1976; Berillon et al., 2011; Druelle et al., 2022). By specifically studying baboons, along with other extant primates, we can enhance our comprehension of the intricate relationships between form and function, which encompass the intrinsic mechanisms involved in the evolutionary transition toward bipedalism. First, we hypothesize that a non-human primate with a quadrupedally-oriented locomotor repertoire should use common muscle synergies in both quadrupedal and bipedal locomotion. Nevertheless, because bipedal walking is an occasional locomotor mode in which keeping balance is a greater challenge than walking quadrupedally, a higher muscle coactivation is expected (as seen in macaques; Higurashi et al., 2019) and, hence, a less complex motor control scheme. Second, the stereotyped pattern observed in humans when walking bipedally (Dominici et al., 2011) should be shared, in some respects, with the one of the baboons walking quadrupedally, at least to deal with the major biomechanical functions inherent to walking.