Hand before foot? Cortical somatotopy suggests manual dexterity is primitive and evolved independently of bipedalism

Abstract

People have long speculated whether the evolution of bipedalism in early hominins triggered tool use (by freeing their hands) or whether the necessity of making and using tools encouraged the shift to upright gait. Either way, it is commonly thought that one led to the other. In this study, we sought to shed new light on the origins of manual dexterity and bipedalism by mapping the neural representations in the brain of the fingers and toes of living people and monkeys. Contrary to the ‘hand-in-glove’ notion outlined above, our results suggest that adaptations underlying tool use evolved independently of those required for human bipedality. In both humans and monkeys, we found that each finger was represented separately in the primary sensorimotor cortex just as they are physically separated in the hand. This reflects the ability to use each digit independently, as required for the complex manipulation involved in tool use. The neural mapping of the subjects’ toes differed, however. In the monkeys, the somatotopic representation of the toes was fused, showing that the digits function predominantly as a unit in general grasping. Humans, by contrast, had an independent neurological representation of the big toe (hallux), suggesting association with bipedal locomotion. These observations suggest that the brain circuits for the hand had advanced beyond simple grasping, whereas our primate ancestors were still general arboreal quadrupeds. This early adaptation laid the foundation for the evolution of manual dexterity, which was preserved and enhanced in hominins. In hominins, a separate adaptation, involving the neural separation of the big toe, apparently occurred with bipedality. This accords with the known fossil evidence, including the recently reported hominin fossils which have been dated to 4.4 million years ago.

Visuomotor control of ankle joint using position vs. force

“…Understanding the motor control characteristics of the lower limb by generalization of findings in upper limb does not seem to be a straightforward task. Some neurophysiological differences between the lower and upper limbs suggest that the performance of tasks involving visuomotor coordination may be different in ankle: (a) the neuro‐circuitries for individuated digit control are evolved differently in lower vs. upper limbs (Hashimoto et al., ), (b) the H‐reflex responses in the lower limb are different from those in the upper limb (Zehr, ), and (c) altering the cutaneous feedback through electrical stimulation affects the performance in visuomotor ankle force‐matching, but not the position‐matching tasks (Choi et al., ). Among similarities, the system‐level neurophysiological signatures such as motor‐related cortical potential are present for both upper limbs (Nasseroleslami, Lakany, & Conway, ,; Nasseroleslami, Lakany, et al., ; Waldert et al., ) and lower limbs (do Nascimento & Farina, ; do Nascimento, Nielsen, & Voigt, ) in position and force control.…”

“…Surprisingly, however, we could not find a similar study at lower extremity that compares the force and position control in the ankle joint or lower extremity. Understanding the lower limb characteristics by generalization of findings in upper limb does not seem to be a straightforward task, given the complex neurophysiological differences between lower and upper limb (Choi, Lundbye‐Jensen, Leukel, & Nielsen, ; Hashimoto et al., ; Zehr, ).…”

Metatarsophalangeal proportions of Homo naledi

“…Additionally, cortical neural mapping suggests that the hand in human and nonhuman primates developed more independently from the foot than previously assumed. 58 If covariation of the hand and feet are inconsistent, the shorter phalanges of H. naledi may indicate a locomotor adaptation unique to H. floresiensis. Shorter toes have been demonstrated to minimally decrease mechanical work of the digital flexor muscles while walking 16 , and drastically decrease the mechanical work while running 15 .…”

Extending mind, visuospatial integration, and the evolution of the parietal lobes in the human genus

“…Humans are a special case, in which bipedal locomotion was associated with increased dexterity and evolution of special handling capacities. Although the relationships between posture and praxis are not clear in terms of evolutionary sequences (e.g., Hashimoto et al, 2013), a full specialized bipedal structure and a patent capacity for complex tooling are strictly associated with the human genus.…”