Cutaneous inputs from perineal region facilitate spinal locomotor activity and modulate cutaneous reflexes from the foot in spinal cats

Merlet, Angèle N.; Harnie, Jonathan; Macovei, Madalina; Doelman, Adam; Gaudreault, Nathaly; Frigon, Alain

doi:10.1002/jnr.24791

Cited by 11 publications

(15 citation statements)

References 85 publications

(212 reference statements)

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“…Cutaneous reflexes from the foot are mediated through polysynaptic pathways and project to several motor pools bilaterally via spinal interneurons intercalated between primary afferents and motoneurons (Lundberg et al, 1977;Pierrot-Deseilligny et al, 1981;Crone et al, 1987;Jankowska, 1992). In our studies, the modulation of cutaneous reflex gain with lumbar or perineal stimulation was independent of background electromyography activity preceding the sensory volley, consistent with premotoneuronal mechanisms (Merlet et al, 2020(Merlet et al, , 2021. Premotoneuronal mechanisms can include gating the transmission of interneurons within or outside the reflex pathway or by changing neurotransmitter release at the primary afferent terminal (e.g., through presynaptic inhibition).…”

Section: Mechanisms Involved In Modulating Spinal Locomotor Cpg Activity and Cutaneous Reflexessupporting

confidence: 79%

“…However, the increase of spinal neuronal excitability is mediated by an undefined mechanism (Pearson and Rossignol, 1991;Harnie et al, 2019). We recently showed, in chronic spinal cats with the hindlimbs restrained, that stimulating the perineal region with vibration or pinch facilitated or triggered rhythmic locomotor-like activity (Merlet et al, 2021). In this study, a base rhythm was initiated by electrically stimulating the superficial peroneal and distal tibial nerves at 0.5 Hz.…”

Section: Facilitation Of the Spinal Locomotor Cpg With Mechanical Stimulation Of The Perineal Regionmentioning

confidence: 76%

“…Recently, we investigated the modulation of cutaneous reflexes from the foot by stimulating the lumbar (Merlet et al, 2020) and perineal (Merlet et al, 2021) regions in chronic spinal cats with the hindlimbs restrained. These cats did not receive a pharmacological treatment.…”

Section: Somatosensory Feedback From Lumbar and Perineal Regions Respectively Increase And Decrease Reflex Gainmentioning

confidence: 99%

“…On the right, the results of reflex responses modulation of selected muscles with lumbar or perineal pinch are illustrated (↑, significant increase; ↓, significant decrease; ↔, non-significant difference in reflex responses). The figure is modified and reproduced with permission from Merlet et al (2020Merlet et al ( , 2021.…”

Section: Mechanisms Involved In Modulating Spinal Locomotor Cpg Activity and Cutaneous Reflexesmentioning

confidence: 99%

“…For instance, inputs from the lumbar skin inhibit hindlimb locomotion (Viala and Buser, 1974;Viala et al, 1978;Frigon et al, 2012b;Hurteau et al, 2015;Merlet et al, 2020), while inputs from the skin of the perineal region facilitate it (Barbeau and Rossignol, 1987;Belanger et al, 1996;Leblond et al, 2003;Langlet et al, 2005;Hochman, 2012;Alluin et al, 2015;Harnie et al, 2019). Our recent work in chronic spinal cats shows that somatosensory inputs from the lumbar and perineal regions, respectively, increase and decrease the gain of cutaneous reflexes from the foot (Merlet et al, 2020(Merlet et al, , 2021. Thus, lumbar and perineal inputs have opposite effects on reflexes, weight support and locomotor activity.…”

Section: Introductionmentioning

confidence: 99%

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Inhibition and Facilitation of the Spinal Locomotor Central Pattern Generator and Reflex Circuits by Somatosensory Feedback From the Lumbar and Perineal Regions After Spinal Cord Injury

2021

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Somatosensory feedback from peripheral receptors dynamically interacts with networks located in the spinal cord and brain to control mammalian locomotion. Although somatosensory feedback from the limbs plays a major role in regulating locomotor output, those from other regions, such as lumbar and perineal areas also shape locomotor activity. In mammals with a complete spinal cord injury, inputs from the lumbar region powerfully inhibit hindlimb locomotion, while those from the perineal region facilitate it. Our recent work in cats with a complete spinal cord injury shows that they also have opposite effects on cutaneous reflexes from the foot. Lumbar inputs increase the gain of reflexes while those from the perineal region decrease it. The purpose of this review is to discuss how somatosensory feedback from the lumbar and perineal regions modulate the spinal locomotor central pattern generator and reflex circuits after spinal cord injury and the possible mechanisms involved. We also discuss how spinal cord injury can lead to a loss of functional specificity through the abnormal activation of functions by somatosensory feedback, such as the concurrent activation of locomotion and micturition. Lastly, we discuss the potential functions of somatosensory feedback from the lumbar and perineal regions and their potential for promoting motor recovery after spinal cord injury.

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Section: Mechanisms Involved In Modulating Spinal Locomotor Cpg Activity and Cutaneous Reflexessupporting

confidence: 79%

Section: Facilitation Of the Spinal Locomotor Cpg With Mechanical Stimulation Of The Perineal Regionmentioning

confidence: 76%

Section: Somatosensory Feedback From Lumbar and Perineal Regions Respectively Increase And Decrease Reflex Gainmentioning

confidence: 99%

Section: Mechanisms Involved In Modulating Spinal Locomotor Cpg Activity and Cutaneous Reflexesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Inhibition and Facilitation of the Spinal Locomotor Central Pattern Generator and Reflex Circuits by Somatosensory Feedback From the Lumbar and Perineal Regions After Spinal Cord Injury

2021

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Control of Mammalian Locomotion by Somatosensory Feedback

Frigon

Akay

Prilutsky

2021

Comprehensive Physiology

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When animals walk overground, mechanical stimuli activate various receptors located in muscles, joints, and skin. Afferents from these mechanoreceptors project to neuronal networks controlling locomotion in the spinal cord and brain. The dynamic interactions between the control systems at different levels of the neuraxis ensure that locomotion adjusts to its environment and meets task demands. In this article, we describe and discuss the essential contribution of somatosensory feedback to locomotion. We start with a discussion of how biomechanical properties of the body affect somatosensory feedback. We follow with the different types of mechanoreceptors and somatosensory afferents and their activity during locomotion. We then describe central projections to locomotor networks and the modulation of somatosensory feedback during locomotion and its mechanisms. We then discuss experimental approaches and animal models used to investigate the control of locomotion by somatosensory feedback before providing an overview of the different functional roles of somatosensory feedback for locomotion. Lastly, we briefly describe the role of somatosensory feedback in the recovery of locomotion after neurological injury. We highlight the fact that somatosensory feedback is an essential component of a highly integrated system for locomotor control.

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Neuromechanical Circuits of the Spinal Motor Apparatus

Nichols

2024

Comprehensive Physiology

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The evolution of mechanisms for terrestrial locomotion has resulted in multi‐segmented limbs that allow navigation on irregular terrains, changing of direction, manipulation of external objects, and control over the mechanical properties of limbs important for interaction with the environment, with corresponding changes in neural pathways in the spinal cord. This article is focused on the organization of these pathways, their interactions with the musculoskeletal system, and the integration of these neuromechanical circuits with supraspinal mechanisms to control limb impedance. It is argued that neural pathways from muscle spindles and Golgi tendon organs form a distributive impedance controller in the spinal cord that controls limb impedance and coordination during responses to external disturbances. These pathways include both monosynaptic and polysynaptic components. Autogenic, monosynaptic pathways serve to control the spring‐like properties of muscles preserving the nonlinear relationship between stiffness and force. Intermuscular monosynaptic pathways compensate for inertial disparities between the inertial properties of limb segments and help to control inertial coupling between joints and axes of rotation. Reciprocal inhibition controls joint stiffness in conjunction with feedforward cocontraction commands. Excitatory force feedback becomes operational during locomotion and increases muscular stiffness to accommodate the higher inertial loads. Inhibitory force feedback is widely distributed among muscles. It is integrated with excitatory pathways from muscle spindles and Golgi tendon organs to determine limb stiffness and interjoint coordination during interactions with the environment. The intermuscular distribution of force feedback is variable and serves to modulate limb stiffness to meet the physical demands of different motor tasks. © 2024 American Physiological Society. Compr Physiol 14:5789‐5838, 2024.

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Cutaneous inputs from perineal region facilitate spinal locomotor activity and modulate cutaneous reflexes from the foot in spinal cats

Cited by 11 publications

References 85 publications

Inhibition and Facilitation of the Spinal Locomotor Central Pattern Generator and Reflex Circuits by Somatosensory Feedback From the Lumbar and Perineal Regions After Spinal Cord Injury

Inhibition and Facilitation of the Spinal Locomotor Central Pattern Generator and Reflex Circuits by Somatosensory Feedback From the Lumbar and Perineal Regions After Spinal Cord Injury

Control of Mammalian Locomotion by Somatosensory Feedback

Neuromechanical Circuits of the Spinal Motor Apparatus

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