Control of Mammalian Locomotion by Somatosensory Feedback

Frigon, Alain; Akay, Turgay; Prilutsky, Boris I.

doi:10.1002/cphy.c210020

Cited by 51 publications

(56 citation statements)

References 844 publications

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“…Note that in the hindlimb-only conditions, the forelimbs are slightly raised on a platform and this potentially increases the load on the hindlimbs. During normal quadrupedal locomotion, cats bear a greater percentage of their bodyweight on their forelimbs because of the weight of the head and neck ( Frigon et al, 2021 ), while in the hindlimb-only conditions with elevated forelimbs, there is a caudal shift of the body’s center of mass and consequently more weight on the hindlimbs. However, our results do not show an increase in the duration of stance consistent with increased load on the hindlimb ( Duysens and Pearson, 1980 ; Conway et al, 1987 ; Bouyer and Rossignol, 2003 ; Frigon, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

“…Spinal animals (i.e., animals with a spinal transection or spinalization) have been instrumental in our understanding of the neural control of locomotion, particularly its spinal control, by comparing the locomotor pattern in the intact and spinal states ( Rossignol et al, 2006 ; Frigon, 2020 ). Spinal animals with a thoracic transection recover hindlimb locomotion due to the presence of spinal locomotor networks, called central pattern generators ( CPGs ), that interact with somatosensory feedback from the limbs ( Rossignol et al, 2006 ; McCrea and Rybak, 2008 ; Rossignol and Frigon, 2011 ; Kiehn, 2016 ; Frigon et al, 2021 ). However, in spinal animals, the forelimbs are often placed on a stationary platform or suspended in the air while the hindlimbs perform locomotor movements ( Forssberg et al, 1980b ; Smith et al, 1982 ; Giuliani and Smith, 1985 ; Robinson and Goldberger, 1986 ; Barbeau and Rossignol, 1987 ; Lovely et al, 1990 ; Leblond et al, 2003 ).…”

Section: Introductionmentioning

confidence: 99%

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State- and Condition-Dependent Modulation of the Hindlimb Locomotor Pattern in Intact and Spinal Cats Across Speeds

Harnie

Audet

Mari

et al. 2022

Front. Syst. Neurosci.

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Locomotion after complete spinal cord injury (spinal transection) in animal models is usually evaluated in a hindlimb-only condition with the forelimbs suspended or placed on a stationary platform and compared with quadrupedal locomotion in the intact state. However, because of the quadrupedal nature of movement in these animals, the forelimbs play an important role in modulating the hindlimb pattern. This raises the question: whether changes in the hindlimb pattern after spinal transection are due to the state of the system (intact versus spinal) or because the locomotion is hindlimb-only. We collected kinematic and electromyographic data during locomotion at seven treadmill speeds before and after spinal transection in nine adult cats during quadrupedal and hindlimb-only locomotion in the intact state and hindlimb-only locomotion in the spinal state. We attribute some changes in the hindlimb pattern to the spinal state, such as convergence in stance and swing durations at high speed, improper coordination of ankle and hip joints, a switch in the timing of knee flexor and hip flexor bursts, modulation of burst durations with speed, and incidence of bi-phasic bursts in some muscles. Alternatively, some changes relate to the hindlimb-only nature of the locomotion, such as paw placement relative to the hip at contact, magnitude of knee and ankle yield, burst durations of some muscles and their timing. Overall, we show greater similarity in spatiotemporal and EMG variables between the two hindlimb-only conditions, suggesting that the more appropriate pre-spinal control is hindlimb-only rather than quadrupedal locomotion.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

State- and Condition-Dependent Modulation of the Hindlimb Locomotor Pattern in Intact and Spinal Cats Across Speeds

Harnie

Audet

Mari

et al. 2022

Front. Syst. Neurosci.

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“…Weak interlimb coupling of neonates may also depend on immature sensory feedback from load signals and hip-position signals 24 , 67 , 68 . Sensory feedback may also contribute to shape neuromuscular modularity, expanding or compressing the number of modules.…”

Section: Discussionmentioning

confidence: 99%

“…We previously compared the results of factorization of neonatal EMG activities during ground stepping and spontaneous kicking 36 . While neonatal stepping is triggered by the contact with the support surface and involves strong sensory signals about limb load and hip extension 24 , 67 , 68 , sensory inputs are not necessary for triggering spontaneous kicking movements, which involve limited feedback about limb load and hip extension. We found that kicking involves activation patterns with a similar dimensionality and waveform as those of more mature locomotion, but they lack a stable association with systematic muscle synergies across movements 36 .…”

Section: Discussionmentioning

confidence: 99%

Complexity of modular neuromuscular control increases and variability decreases during human locomotor development

et al. 2022

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When does modular control of locomotion emerge during human development? One view is that modularity is not innate, being learnt over several months of experience. Alternatively, the basic motor modules are present at birth, but are subsequently reconfigured due to changing brain-body-environment interactions. One problem in identifying modular structures in stepping infants is the presence of noise. Here, using both simulated and experimental muscle activity data from stepping neonates, infants, preschoolers, and adults, we dissect the influence of noise, and identify modular structures in all individuals, including neonates. Complexity of modularity increases from the neonatal stage to adulthood at multiple levels of the motor infrastructure, from the intrinsic rhythmicity measured at the level of individual muscles activities, to the level of muscle synergies and of bilateral intermuscular network connectivity. Low complexity and high variability of neuromuscular signals attest neonatal immaturity, but they also involve potential benefits for learning locomotor tasks.

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“…We suggest that stimulation of cutaneous and proprioceptive afferents in the distal tibial nerve provides functionally meaningful motion-dependent sensory feedback, and stimulation responses depend on limb conditions. Keywords: tactile sensation, distal tibial nerve stimulation, quadrupedal locomotion Somatosensory motion-dependent feedback is a critical component of the locomotor control system, and terrestrial legged animals from insects to humans have evolved similar sensory modalities and control mechanisms that provide for stable and efficient locomotion; see recent reviews (Edwards & Prilutsky, 2017;Frigon et al, 2021;Tuthill & Azim, 2018). Specifically, length-and loaddependent sensory feedback entrains locomotor rhythm (Kriellaars et al, 1994;Pearson & Collins, 1993) and regulates the level of muscle or motoneuronal activity (af Klint et al, 2010;Akay et al, 2004;Chung et al, 2015;Guertin et al, 1995;Lam & Pearson, 2002) and timing of the transitions between the swing (flexor) and stance (extensor) phases of the locomotor cycle (Schomburg et al, 1998;Stecina et al, 2005).…”

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confidence: 99%

Electrical Stimulation of Distal Tibial Nerve During Stance Phase of Walking May Reverse Effects of Unilateral Paw Pad Anesthesia in the Cat

Park

Klishko

et al. 2023

Motor Control

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Cutaneous feedback from feet is involved in regulation of muscle activity during locomotion, and the lack of this feedback results in motor deficits. We tested the hypothesis that locomotor changes caused by local unilateral anesthesia of paw pads in the cat could be reduced/reversed by electrical stimulation of cutaneous and proprioceptive afferents in the distal tibial nerve during stance. Several split-belt conditions were investigated in four adult female cats. In addition, we investigated the effects of similar distal tibial nerve stimulation on overground walking of one male cat that had a transtibial, bone-anchored prosthesis for 29 months and, thus, had no cutaneous/proprioceptive feedback from the foot. In all treadmill conditions, cats walked with intact cutaneous feedback (control), with right fore- and hindpaw pads anesthetized by lidocaine injections, and with a combination of anesthesia and electrical stimulation of the ipsilateral distal tibial nerve during the stance phase at 1.2× threshold of afferent activation. Electrical stimulation of the distal tibial nerve during the stance phase of walking with anesthetized ipsilateral paw pads reversed or significantly reduced the effects of paw pad anesthesia on several kinematic variables, including lateral center of mass shift, cycle and swing durations, and duty factor. We also found that stimulation of the residual distal tibial nerve in the prosthetic hindlimb often had different effects on kinematics compared with stimulation of the intact hindlimb with paw anesthetized. We suggest that stimulation of cutaneous and proprioceptive afferents in the distal tibial nerve provides functionally meaningful motion-dependent sensory feedback, and stimulation responses depend on limb conditions.

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Control of Mammalian Locomotion by Somatosensory Feedback

Cited by 51 publications

References 844 publications

State- and Condition-Dependent Modulation of the Hindlimb Locomotor Pattern in Intact and Spinal Cats Across Speeds

State- and Condition-Dependent Modulation of the Hindlimb Locomotor Pattern in Intact and Spinal Cats Across Speeds

Complexity of modular neuromuscular control increases and variability decreases during human locomotor development

Electrical Stimulation of Distal Tibial Nerve During Stance Phase of Walking May Reverse Effects of Unilateral Paw Pad Anesthesia in the Cat

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