Integration of feedforward and feedback control in the neuromechanics of vertebrate locomotion: a review of experimental, simulation and robotic studies

Abstract

Animal locomotion is the result of complex and multi-layered interactions between the nervous system, the musculo-skeletal system and the environment. Decoding the underlying mechanisms requires an integrative approach. Comparative experimental biology has allowed researchers to study the underlying components and some of their interactions across diverse animals. These studies have shown that locomotor neural circuits are distributed in the spinal cord, the midbrain and higher brain regions in vertebrates. The spinal cord plays a key role in locomotor control because it contains central pattern generators (CPGs) – systems of coupled neuronal oscillators that provide coordinated rhythmic control of muscle activation that can be viewed as feedforward controllers – and multiple reflex loops that provide feedback mechanisms. These circuits are activated and modulated by descending pathways from the brain. The relative contributions of CPGs, feedback loops and descending modulation, and how these vary between species and locomotor conditions, remain poorly understood. Robots and neuromechanical simulations can complement experimental approaches by testing specific hypotheses and performing what-if scenarios. This Review will give an overview of key knowledge gained from comparative vertebrate experiments, and insights obtained from neuromechanical simulations and robotic approaches. We suggest that the roles of CPGs, feedback loops and descending modulation vary among animals depending on body size, intrinsic mechanical stability, time required to reach locomotor maturity and speed effects. We also hypothesize that distal joints rely more on feedback control compared with proximal joints. Finally, we highlight important opportunities to address fundamental biological questions through continued collaboration between experimentalists and engineers.

Fine-grained descending control of steering in walkingDrosophila

“…Specifically, the rhythmic limb movement pattern is intrinsic to the vertebrate spinal cord 1,2 or the arthropod ventral nerve cord [3][4][5][6][7] . Meanwhile, descending signals from the brain to the cord are required to start or stop locomotion, modulate speed, or change direction in both vertebrates and arthropods [8][9][10][11][12] . Yet the brain's role in locomotor control is not necessarily limited to general high-level commands: blocking descending signals from the brain can also alter the details of limb coordination during walking in both vertebrates [13][14][15] and arthropods 7,16 , and stimulation of specific descending tracts can produce excitation or inhibition of muscle groups in multiple limbs [17][18][19][20][21] .…”

Sensory Feedback and Central Neuronal Interactions in Mouse Locomotion

“…Limb coordination during locomotion, and hence the locomotor gait, can depend on, and be influenced by, both central neural interactions between RG circuits controlling each limb and multiple feedback signals to the RGs reflecting interactions between the neural controller and mechanical components of the system. The latter creates additional interactions between the RGs mediated by peripheral feedback [17, 18, 20, 22, 97, 98]. Since both these interactions depend on the locomotor speed, limb coordination and therefore locomotor gaits are also speed dependent.…”

“…However, during actual locomotion, sensory feedback from the limbs, which reflects the state of limb muscles, limb/body mechanics, and interactions with the environment, can modulate or even override the locomotor oscillations generated by the spinal circuits and their coordination. The specific interactions between the central controller and sensory feedback, as well as the role of different feedback types in regulating locomotor speed, gait, postural stability, and movement direction under different experimental conditions, remain contradictory and poorly understood [17][18][19][20][21][22][23]. Moreover, some theories almost exclusively rely on the critical role of sensory feedback in the timing of locomotor phase transitions and interlimb coordination [24][25][26][27], hence devaluing the role of central mechanisms.…”

Two modes in the velocity statistics in cautious walks of laboratory rodents

“…Substituting these expressions into (14) and making the Fourier transform in accordance with the Wiener-Khinchin theorem [51,52] we obtain the correlation function of the acceleration…”

“…the reviews in [11,12]. Evolutionary cephalization facilitated goaldirected locomotive strategies [13,14]. A search for a randomly-distributed resources might include a Brownian strategy in mammalian and avian species [15][16][17][18], or its modifications such as correlated random walks [19][20][21].…”