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Control of Mammalian Locomotion by Somatosensory Feedback

Alain Frigon, Turgay Akay, Boris I. Prilutsky

10.1002/cphy.c210020

Source: Volume 12, Issue 1, January 2022

Published online: December 2021

Full Article on Wiley Online Library



Abstract

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. © 2021 American Physiological Society. Compr Physiol 11:1‐71, 2021.

Figure 1. Figure 1. Neural control of locomotion . (A) The half‐center model is composed of populations of last‐order interneurons that control extensor (In‐E) and flexor (In‐F) motoneurons. MN‐E and MN‐F represent extensor and flexor motoneurons, respectively. The In‐E and In‐F populations receive excitatory inputs from contralateral (coFRA) and ipsilateral (iFRA) flexor reflex afferents, respectively, and these interneuron populations mutually inhibit each other. FRAs have been used to characterize a collection of high‐threshold afferents from muscle, joint, and cutaneous receptors involved in generating ipsilateral limb flexion (and crossed extension). However, stimulating FRAs produce excitatory and inhibitory responses in both ipsilateral flexors and extensors as well as muscles of the other limbs and the term can lead to confusion. Based on Jankowska E, et al., 1967 440 . (B) The unit burst generator model originally proposed by Grillner 337 . EDB, extensor digitorum brevis. Modified, with permission, from Grillner S, et al., 2008 343 . (C) The two‐layer central pattern generator model separating rhythm generation (RG) and pattern formation (PF). Last‐order extensor (PF‐E) and flexor (PF‐F) populations of interneurons at the PF level control extensor (MN‐E) and flexor (MN‐F) motoneuron pools, respectively. PF‐E and PF‐F mutually inhibit each other via inhibitory interneurons (InPF‐E and InPF‐F). The pattern formation level receives inputs from extensor (RG‐E) and flexor (RG‐F) populations of interneurons located at the rhythm generation level. The RG‐E and RG‐F populations can mutually excite or inhibit each other. Somatosensory feedback projects to neurons at the RG and PF levels as well as motoneurons. Motoneurons also receive inputs from Ia inhibitory interneurons (Ia‐E and Ia‐F) and motoneuron collaterals project to Renshaw cells (R‐E and R‐F). Adapted, with permission, from Rybak IA, et al., 2006 729,730 . (D) Schematic representation of the neural control of interlimb coordination. A distinct spinal locomotor CPG controls each limb. Commissural interneurons ensure left‐right coordination at cervical and lumbar levels. Descending and ascending propriospinal pathways, with homolateral and diagonal projections, coordinate cervical and lumbar CPGs. Propriospinal pathways can consist of neurons with long or short axonal projections. Supraspinal inputs and somatosensory feedback from the limbs access spinal CPGs via commissural and propriospinal pathways. Reproduced, with permission, from Frigon A, 2017 275 . Arrows represent excitatory or inhibitory influences. E, extensor; F, flexor; LF, left forelimb; LH, left hindlimb; RF, right forelimb; RH, right hindlimb.
Figure 2. Figure 2. Examples of mammalian gaits . Examples of quadrupedal symmetric gaits classified based on the duty cycle (the horizontal axis in the graph) and the phase difference between the homolateral hindlimb and forelimb footfalls (vertical axis). Examples of symmetric gaits include walking with a lateral sequence of footfalls of the pygmy hippopotamus with a lateral limb support sequence (top left); three running gaits of the horse, including a pace with in‐phase 2‐beat movements of the homolateral limbs (top right), trot with in‐phase 2‐beat movements of the contralateral fore‐ and hindlimbs (middle bottom) and a 4‐beat lateral sequence gait with a single foot on the ground and the other limbs in swing (middle top); a 4‐beat diagonal sequence gait with a single foot on the ground and the other limbs in swing in the duiker, an African antelope (bottom right); and walking with a diagonal sequence of footfalls in the monkey. Modified, with permission, from Hildebrand M, 1989 374 .
Figure 3. Figure 3. Support phases during walking in the cat and related static and dynamic stability measures . (A) Limb support phases (top), the corresponding cat body configurations with the base of support (in gray), paw prints, center of mass (circles), and extrapolated center of mass (diamonds) shown for each limb support phase during cat overground walking. Reproduced, with permission, from Farrell BJ, et al., 2014 251 . (B) Support phases during treadmill walking for the left hindlimb (LH), left forelimb (LF), right hindlimb (RH), and right forelimb (RF) shown by horizontal lines at bottom. The traces correspond to the position of the center of mass (CoM), extrapolated center of mass (xCoM), and the center of pressure (CoP) in the left‐right direction as a function of time. Vertical shaded rectangles correspond to the 8 support phases. Reproduced, with permission, from Park H, et al., 2019 636 .
Figure 4. Figure 4. Ground reaction forces of different quadrupedal species and humans during locomotion . In quadrupeds of different sizes from a mouse to a giraffe, vertical ground reaction force (GRF) applied to the forelimbs is typically greater than the GRF applied to the hindlimbs. The forelimbs generate larger breaking force impulses than accelerating impulses in the anterior‐posterior direction. The accelerating force impulses of the hindlimbs are larger than breaking ones. In all panels except for human walking, solid lines are vertical forces, dashed lines are anterior‐posterior forces, and dashed lines with dots are medio‐lateral forces (medio‐lateral ground reaction applied to the foot is directed toward the body, that is, the foot applies force on the ground in the opposite outward direction). From top left to bottom right: GRFs of walking mouse, Modified from 156 , GRFs of trotting rat, modified from 591 , GRFs of walking cat 251 , normal and anterior‐posterior forces during level, upslope and downslope walking in humans, modified from 487 , GRFs of trotting horse, modified from 157 and GRFs of walking giraffe, modified from 66 . BW, bodyweight; LF, left forelimb; LH, left hindlimb; RF, right forelimb; RH, right hindlimb.
Figure 5. Figure 5. Schematic representation of ensemble activity of muscle afferents . The figure shows afferent activity recorded in freely walking cats (red lines) and computed using a neuromechanical model relating afferent activity to instantaneous muscle fascicle length and velocity and tendon force (blue lines). Length‐related spindle primary (Ia) and secondary (II) afferents from ankle (tibialis anterior) and knee (biceps femoris posterior) flexors demonstrate increased activity at the swing‐to‐stance transition, while spindle secondary afferents from hip flexors (rectus femoris and medial sartorius) show increased activity at the stance‐to‐swing transition. These patterns of activity are consistent with muscle fascicle length changes. Length‐related activity of spindle afferents and force‐related activity of GTO afferents of ankle (triceps surae, soleus, gastrocnemius) and knee (vasti and rectus femoris) extensors is high during the stance phase and corresponds to high EMG activity of these muscles in stance. High activity of GTO afferents of the knee flexor‐hip extensor hamstrings at phase transitions also corresponds to EMG activity pattern of this muscle. BFP, posterior biceps femoris; GS, gastrocnemius; HAM, hamstrings; RF, rectus femoris; SOL, soleus; SrtM, medial sartorius TA, tibialis anterior; TS, triceps surae; [1] Prochazka and Gorassini 692 ; [2] and [5], Loeb, Duysens 503 ; [3, 4] and [6], Loeb et al. 504,505,506 ; [7] Loeb 500 . Computed afferent activity is taken from 686 . Adapted, with permission, from Prilutsky BI, et al., 2016 686 .
Figure 6. Figure 6. Projections from single group Ia afferent to neuronal targets of spinal cord . The figure shows the trajectory of axon collaterals of a muscle spindle primary afferent (group Ia) from the medial gastrocnemius intra‐axonally labeled with horseradish peroxidase. Colored circles indicate the location of five populations of target cells contacted by terminal branches of the group Ia afferent. Approximate locations of spinal cord laminae are shown (from Roman numerals II‐X). DSCT, dorsal spinocerebellar tract; VSCT, ventral spinocerebellar tract. Adapted and reproduced, with permission, from Jankowska E, 2015 435 ; Ishizuka N, et al., 1979 419 .
Figure 7. Figure 7. Muscle afferent projections in the rat spinal cord . Figure shows contour maps of varicosities from three afferents of each class (Group Ia, II, and Ib). Contour maps created by calculating the density of varicosities and outlining areas above a certain threshold. Approximate locations of spinal cord laminae are shown. Modified, with permission, from Vincent JA, et al., 2017 835 .
Figure 8. Figure 8. Task‐dependent modulation of somatosensory feedback . Effects of manually dorsiflexing the ankle (∼5°) during spontaneous (A) fictive locomotion and (B) fictive scratching in a decerebrate curarized cat. Figure shows activity from extensor and flexor nerves. EDL, extensor digitorum longus; MG, medial gastrocnemius; SmAB, semimembranosus‐anterior biceps; TA, tibialis anterior. Modified, with permission, from Frigon A and Gossard JP, 2010 282 .
Figure 9. Figure 9. Phase‐dependent modulation of cutaneous reflexes . Phase‐and speed‐dependent modulation of cutaneous reflexes evoked by electrically stimulating the superficial peroneal nerve (single 0.2 ms pulse at 1.2 times the motor threshold) in (A) semitendinosus, (B) vastus lateralis and (C) lateral gastrocnemius at a treadmill speed of 0.4 m/s in a spinal cat. Cutaneous reflexes are separated into 10 bins. Rectified EMG waveforms obtained with stimulation are separated into 10 bins (average of 5–17 cycles per bin). The black lines show the background level of EMG in each bin (average of ∼90 control cycles). The EMG waveform shown vertically on the right of each panel is the rectified activity of the muscle across the normalized cycle. Modified, with permission, from Hurteau MF, et al., 2017 407 .
Figure 10. Figure 10. Phase‐dependent modulation of postsynaptic potentials evoked by stimulating extensor and flexor muscle afferents at group I strength during fictive locomotion . (A) Nerves to plantaris (Pl) and sartorius (Srt) muscles were stimulated at group I strength during spontaneous fictive locomotion in a decerebrate curarized cat. Intracellular recordings from antidromically identified motoneurons were made with glass micropipettes filled with QX‐314. The type (i.e., inhibitory or excitatory) of last‐order interneuron activated within a given reflex pathway can be inferred by the sign of the postsynaptic potential recorded in the motoneuron. (B) During a fictive locomotor episode, the 2 nerves were stimulated with high frequency and short trains (6 pulses at 200 Hz) in alternation, with an interval of 150 to 250 ms between nerve stimulations. From top to bottom: Evoked responses tilted 90° evoked by Srt and Pl nerve stimulation given in alternation; intracellular membrane potential oscillations in the SmAB motoneuron showing the locomotor‐drive potential and superimposed evoked responses; ENGs from extensors, semimembranosus‐anterior biceps (SmAB), and lateral gastrocnemius‐soleus (LGS) and from a flexor, tibialis anterior (TA). The locomotor cycle was divided into extension and flexion phases according to the extensor ENG onset and offsets. (C) Postsynaptic potentials evoked by stimulating Srt and Pl nerves were divided and averaged into extension and flexion phases. Data were recorded in Jean‐Pierre Gossard's lab at the Université de Montréal.
Figure 11. Figure 11. Presynaptic inhibition through primary afferent depolarization . The figure shows synaptic contact between a primary afferent and a postsynaptic neuron. Two GABAergic interneurons make axo‐axonic contacts on the primary afferent. One GABAergic interneuron receives converging glutamatergic inputs from a group I afferent and from a CPG neuron while the other GABAergic interneuron receives input from a reticulospinal neuron. During locomotion, the group I afferent and CPG neuron depolarize their target GABAergic interneuron, leading to the release of GABA. GABA binds to GABA A ionotropic receptors on the primary afferent and opens Cl − channels. Cl − exits the primary afferent leading to a depolarization (PAD, primary afferent depolarization) and an electrotonic potential that travels in both directions. The antidromic PAD collides with the action potential coming from the periphery, reducing the orthodromic response and preventing release of glutamate at the primary afferent terminal. The electrotonic potential traveling in the orthodromic direction weakens in magnitude the further it travels and as it reaches the terminal, it is too weak to affect transmitter release.
Figure 12. Figure 12. Modulation of somatosensory feedback and its interactions with central locomotor networks . The figure shows potential mechanisms and interactions modulating inputs from a group Ib afferent of an ankle extensor. Upon entering the spinal cord, the Ib afferent makes synaptic contacts with neurons of the dorsal spinocerebellar tract (DSCT), the spinal locomotor CPG, represented as extensor and flexor half‐centers, as well as inhibitory and excitatory last‐order interneurons that project to ankle extensor motoneurons. The Ib afferent also ascends to brainstem nuclei that transmit the information to the cerebellum, thalamus, and cerebral cortex. At rest, the disynaptic inhibitory pathway is open and the excitatory pathway is inhibited. During locomotion, the spinal CPG inhibits the inhibitory pathway and releases the excitatory pathway from inhibition through disinhibition. At the same time, various supraspinal structures interact dynamically with each other and with spinal circuits, such as the spinal CPG and local reflex circuits.
Figure 13. Figure 13. Proprioceptive feedback and mouse genetics . (A) Selective removal of muscle spindles in Egr3‐KO mice occurs through loss of neurotrophin 3 (NT3) expression in the muscle spindles resulting in their degeneration postnatally. (B) Proprioceptive afferent neurons are selectively removed by making them selectively express the highly toxic DTA using the calcium‐binding protein Parvalbumin (Pv) and the transcription factor Isl2, both genes collectively expressed in proprioceptive afferents only. (C) Alternatively, proprioceptive afferent neurons can be made susceptible to the diphtheria toxin (DTX) by making them express the gene that encodes the diphtheria toxin receptor (DTR), normally not expressed in mice. In these mice, systemic injection of DTX results in acute removal of the proprioceptors. (D) The gene that encodes the DTR in a cre‐dependent manner can be postnatally delivered via adeno associated virus (AAV) injections into selected muscles. Later, as in (C), proprioceptive afferents only from the AAV injected muscles can be destroyed by systemic injection of DTX.
Figure 14. Figure 14. Hill‐type muscle model and its properties . (A) Three‐element Hill‐type model. CE, contractile element; PE, parallel elastic element; T, tendon; m, mass of muscle fascicles. (B) Normalized force‐length relationship of the contractile element fully activated and producing force isometrically, that is, without length change. Force is normalized to the maximum muscle force developed by the fully activated muscle at its optimal length. Length is normalized to the optimal muscle fascicle length. (C) Normalized force‐velocity relationship of the contractile element. Velocity is normalized to the maximum shortening velocity. Positive velocity corresponds to shortening. (D) Normalized tendon force‐length relationship. Parameters F Tnl , L Tnl and L T Max are empirical constants; L To is the resting (slack) tendon length. Adapted, with permission, from Prilutsky BI, et al., 2016 686 .
Figure 15. Figure 15. Pyridoxine intoxications reveal that large diameter somatosensory afferents contribute to postural control . (A) Schematic of the experimental set‐up. Filled circles represent kinematic markers. The antero‐posterior (AP) stance distance is the horizontal distance between the wrist and ankle joints. Forelimb, hindlimb, and trunk axis indicated by dashed lines. Reproduced and modified, with permission, from Fung J and Macpherson JM, 1999 293 . (B) Rectified averaged EMG activity of the gluteus medius and biceps femoris medial head before (control) and 7 days after pyridoxine intoxication, which destroys large‐diameter somatosensory afferents, in one cat with translation of the support surface at 240°. The dashed vertical line indicates the onset of platform acceleration. Under each trace, the arrows indicate response onset in control trials and at day 7. (C) Amplitude maximum initial displacement of the CoM and time of maximum displacement in relation to platform translation at 240°. Error bars indicate SE. **Significantly different from control values ( P  < 0.001, one‐way ANOVA). (B,C) Reproduced and modified, with permission, from Stapley PJ, et al., 2002 791 .
Figure 16. Figure 16. Somatosensory feedback is required for proper paw placement during skilled locomotion . (A) Cat stepping on a horizontal ladder before (control) and after a complete cutaneous denervation of the hindpaws. Based on, with permission, Bouyer LJ and Rossignol S, 2003 93 . (B) Egr3 mutant mice make more errors during walking on a horizontal ladder, determined as more frequent foot droppings between rungs than in wild types. Each bar indicates the number of steps that landed on a rung (black bars) or missed the rung (red bars) counted during one run. Each set of bar represents a run from different mouse ( n  = 13 for wild type and n  = 15 for Egr3 mutants). Based on, with permission, Akay T, et al., 2014 10 .
Figure 17. Figure 17. The loss of muscle spindle feedback in mice impairs swimming but not treadmill locomotion . Locomotor pattern gradually degrades with removal of proprioceptive feedback. (A) Chronic EMG recordings were made during treadmill locomotion and swimming in wild‐type and Egr3 mutants that lack functional muscle spindle feedback. (B) Bar diagram illustrating the activity of flexor (red) and extensor (blue) muscles during treadmill walking and swimming in wild‐type ( n  = 16 for walking and n  = 14 for swimming) and Egr3 mutant ( n  = 15 for walking and swimming) mice. Each horizontal bar is the average EMG activity in a normalized locomotor cycle (between successive swing or iliopsoas burst onsets for walking and swimming, respectively). GM, gluteus maximum; IP, iliopsoas; St, semitendinosus; TA, tibialis anterior; VL, vastus lateralis. Based on, with permission, Akay T, et al., 2014 10 .
Figure 18. Figure 18. Effect of stimulating muscle afferents during spontaneous fictive locomotion in decerebrate curarized cats . The figure shows the effect of stimulating the plantaris (Pl) nerve at group I strength and the sartorius (Srt) nerve at group II strength on the raw ENG bursts of activity during spontaneous fictive locomotion. Stimulation of the Pl nerve during (A) mid‐flexion resets the rhythm to extension while stimulation during (B) late extension prolongs the extensor burst. Stimulation of the Srt nerve during (C) early flexion resets the rhythm to extension while stimulation during (D) mid‐ to late extension has no visible effect. LGS, lateral gastrocnemius‐soleus; SmAB, semimembranosus‐anterior biceps; T, threshold; TA, tibialis anterior. Reproduced and modified, with permission, from Frigon A, et al., 2010 288 .
Figure 19. Figure 19. Proprioceptive feedback from extensor muscles contributes to the magnitude of extensor activity . (A) When the hindlimb of a decerebrate cat steps in a hole during treadmill locomotion, the EMG activity in ankle (LG, lateral gastrocnemius) and knee extensor (VM, vastus medialis) muscles is reduced. The shaded area indicates the time the foot entered the hole. (B) Loading ankle extensor muscles during foot‐in‐hole trials restored normal levels of EMG activity in ankle extensor muscles. The shaded area indicates the time the foot entered the hole without (top) and with (bottom) load applied to the Achilles tendon. Adapted, with permission, from Hiebert GW and Pearson KG, 1999 370 .
Figure 20. Figure 20. Cutaneous inputs regulate muscle activity and alter limb trajectory in a phase‐dependent manner . (A) The effects of stimulating the superficial radial (SR) and superficial peroneal (SP) nerves on the EMG activity of selected muscles and the phases of the four limbs during treadmill locomotion at 0.4 m/s in an intact cat. The SR and SP nerves were stimulated during mid‐stance and mid‐swing of the homonymous limb. The shaded area indicates the period of stimulation (25 pulses of 0.2 ms duration at 200 Hz and at 1.2 times the motor threshold). (B) Kinematic reconstruction of the forelimb (top panels) and hindlimb (bottom panels) without (control) and with stimulation during stance and swing. Note that in the top panels the left SR was stimulated while in the bottom panels the right SP was stimulated. Unpublished data from Frigon lab. BB, biceps brachii; ECU, extensor carpi ulnaris; FCU, flexor carpi ulnaris; GL, gastrocnemius lateralis; L, left; F, forelimb; H, hindlimb; R, right; Srt, anterior sartorius; ST, stance; TA, tibialis anterior; TRI, triceps brachii.
Figure 21. Figure 21. Cutaneous inputs regulate inter‐joint coordination during locomotion . The figure shows short‐latency pathways from cutaneous afferents of the superficial peroneal (SP) nerve to different hindlimb motoneurons during the flexion phase of fictive locomotion. The central pattern generator (CPG) is shown with mutually inhibiting extensor (E) and flexor (F) parts. The CPG can phasically modulate interneurons mediating di‐ and trisynaptic excitation of hindlimb motoneurons from SP afferents. The inhibitory pathway to ankle extensor motoneurons observed at rest (last‐order inhibitory interneuron In‐2) is inhibited by the spinal locomotor CPG. Ex‐1 and Ex‐2, excitatory interneurons 1 and 2; In‐1 and In‐2, inhibitory interneurons 1 and 2. Reproduced and modified, with permission, from Quevedo J, et al., 2000 705 .
Figure 22. Figure 22. Interlimb reflexes coordinate the four limbs during locomotion . Schematic of reflex pathways and main responses during stance and swing evoked by SP nerve stimulation. (A) Upon entering the spinal cord, primary afferents from the SP nerve contact (i) interneurons that project within the hemisegment (homonymous responses), (ii) commissural interneurons that project contralaterally (crossed responses), and (iii) ascending propriospinal neurons with their main axonal projections terminating ipsilaterally (homolateral responses) or on the other side (diagonal responses). Diagonal pathways cross at various segments along the length of the spinal cord and include collaterals from homolateral pathways that also project contralaterally. (B) Panels show the main pattern of forelimb and hindlimb responses evoked with SP nerve stimulation when the different limbs are in mid‐swing or mid‐stance. Responses shaded in dark blue represent excitatory responses while those in red represent inhibitory responses. Responses are aligned to the start of the stimulation. Adapted, with permission, from Hurteau MF, et al., 2018 408 .


Figure 1. Neural control of locomotion . (A) The half‐center model is composed of populations of last‐order interneurons that control extensor (In‐E) and flexor (In‐F) motoneurons. MN‐E and MN‐F represent extensor and flexor motoneurons, respectively. The In‐E and In‐F populations receive excitatory inputs from contralateral (coFRA) and ipsilateral (iFRA) flexor reflex afferents, respectively, and these interneuron populations mutually inhibit each other. FRAs have been used to characterize a collection of high‐threshold afferents from muscle, joint, and cutaneous receptors involved in generating ipsilateral limb flexion (and crossed extension). However, stimulating FRAs produce excitatory and inhibitory responses in both ipsilateral flexors and extensors as well as muscles of the other limbs and the term can lead to confusion. Based on Jankowska E, et al., 1967 440 . (B) The unit burst generator model originally proposed by Grillner 337 . EDB, extensor digitorum brevis. Modified, with permission, from Grillner S, et al., 2008 343 . (C) The two‐layer central pattern generator model separating rhythm generation (RG) and pattern formation (PF). Last‐order extensor (PF‐E) and flexor (PF‐F) populations of interneurons at the PF level control extensor (MN‐E) and flexor (MN‐F) motoneuron pools, respectively. PF‐E and PF‐F mutually inhibit each other via inhibitory interneurons (InPF‐E and InPF‐F). The pattern formation level receives inputs from extensor (RG‐E) and flexor (RG‐F) populations of interneurons located at the rhythm generation level. The RG‐E and RG‐F populations can mutually excite or inhibit each other. Somatosensory feedback projects to neurons at the RG and PF levels as well as motoneurons. Motoneurons also receive inputs from Ia inhibitory interneurons (Ia‐E and Ia‐F) and motoneuron collaterals project to Renshaw cells (R‐E and R‐F). Adapted, with permission, from Rybak IA, et al., 2006 729,730 . (D) Schematic representation of the neural control of interlimb coordination. A distinct spinal locomotor CPG controls each limb. Commissural interneurons ensure left‐right coordination at cervical and lumbar levels. Descending and ascending propriospinal pathways, with homolateral and diagonal projections, coordinate cervical and lumbar CPGs. Propriospinal pathways can consist of neurons with long or short axonal projections. Supraspinal inputs and somatosensory feedback from the limbs access spinal CPGs via commissural and propriospinal pathways. Reproduced, with permission, from Frigon A, 2017 275 . Arrows represent excitatory or inhibitory influences. E, extensor; F, flexor; LF, left forelimb; LH, left hindlimb; RF, right forelimb; RH, right hindlimb.


Figure 2. Examples of mammalian gaits . Examples of quadrupedal symmetric gaits classified based on the duty cycle (the horizontal axis in the graph) and the phase difference between the homolateral hindlimb and forelimb footfalls (vertical axis). Examples of symmetric gaits include walking with a lateral sequence of footfalls of the pygmy hippopotamus with a lateral limb support sequence (top left); three running gaits of the horse, including a pace with in‐phase 2‐beat movements of the homolateral limbs (top right), trot with in‐phase 2‐beat movements of the contralateral fore‐ and hindlimbs (middle bottom) and a 4‐beat lateral sequence gait with a single foot on the ground and the other limbs in swing (middle top); a 4‐beat diagonal sequence gait with a single foot on the ground and the other limbs in swing in the duiker, an African antelope (bottom right); and walking with a diagonal sequence of footfalls in the monkey. Modified, with permission, from Hildebrand M, 1989 374 .


Figure 3. Support phases during walking in the cat and related static and dynamic stability measures . (A) Limb support phases (top), the corresponding cat body configurations with the base of support (in gray), paw prints, center of mass (circles), and extrapolated center of mass (diamonds) shown for each limb support phase during cat overground walking. Reproduced, with permission, from Farrell BJ, et al., 2014 251 . (B) Support phases during treadmill walking for the left hindlimb (LH), left forelimb (LF), right hindlimb (RH), and right forelimb (RF) shown by horizontal lines at bottom. The traces correspond to the position of the center of mass (CoM), extrapolated center of mass (xCoM), and the center of pressure (CoP) in the left‐right direction as a function of time. Vertical shaded rectangles correspond to the 8 support phases. Reproduced, with permission, from Park H, et al., 2019 636 .


Figure 4. Ground reaction forces of different quadrupedal species and humans during locomotion . In quadrupeds of different sizes from a mouse to a giraffe, vertical ground reaction force (GRF) applied to the forelimbs is typically greater than the GRF applied to the hindlimbs. The forelimbs generate larger breaking force impulses than accelerating impulses in the anterior‐posterior direction. The accelerating force impulses of the hindlimbs are larger than breaking ones. In all panels except for human walking, solid lines are vertical forces, dashed lines are anterior‐posterior forces, and dashed lines with dots are medio‐lateral forces (medio‐lateral ground reaction applied to the foot is directed toward the body, that is, the foot applies force on the ground in the opposite outward direction). From top left to bottom right: GRFs of walking mouse, Modified from 156 , GRFs of trotting rat, modified from 591 , GRFs of walking cat 251 , normal and anterior‐posterior forces during level, upslope and downslope walking in humans, modified from 487 , GRFs of trotting horse, modified from 157 and GRFs of walking giraffe, modified from 66 . BW, bodyweight; LF, left forelimb; LH, left hindlimb; RF, right forelimb; RH, right hindlimb.


Figure 5. Schematic representation of ensemble activity of muscle afferents . The figure shows afferent activity recorded in freely walking cats (red lines) and computed using a neuromechanical model relating afferent activity to instantaneous muscle fascicle length and velocity and tendon force (blue lines). Length‐related spindle primary (Ia) and secondary (II) afferents from ankle (tibialis anterior) and knee (biceps femoris posterior) flexors demonstrate increased activity at the swing‐to‐stance transition, while spindle secondary afferents from hip flexors (rectus femoris and medial sartorius) show increased activity at the stance‐to‐swing transition. These patterns of activity are consistent with muscle fascicle length changes. Length‐related activity of spindle afferents and force‐related activity of GTO afferents of ankle (triceps surae, soleus, gastrocnemius) and knee (vasti and rectus femoris) extensors is high during the stance phase and corresponds to high EMG activity of these muscles in stance. High activity of GTO afferents of the knee flexor‐hip extensor hamstrings at phase transitions also corresponds to EMG activity pattern of this muscle. BFP, posterior biceps femoris; GS, gastrocnemius; HAM, hamstrings; RF, rectus femoris; SOL, soleus; SrtM, medial sartorius TA, tibialis anterior; TS, triceps surae; [1] Prochazka and Gorassini 692 ; [2] and [5], Loeb, Duysens 503 ; [3, 4] and [6], Loeb et al. 504,505,506 ; [7] Loeb 500 . Computed afferent activity is taken from 686 . Adapted, with permission, from Prilutsky BI, et al., 2016 686 .


Figure 6. Projections from single group Ia afferent to neuronal targets of spinal cord . The figure shows the trajectory of axon collaterals of a muscle spindle primary afferent (group Ia) from the medial gastrocnemius intra‐axonally labeled with horseradish peroxidase. Colored circles indicate the location of five populations of target cells contacted by terminal branches of the group Ia afferent. Approximate locations of spinal cord laminae are shown (from Roman numerals II‐X). DSCT, dorsal spinocerebellar tract; VSCT, ventral spinocerebellar tract. Adapted and reproduced, with permission, from Jankowska E, 2015 435 ; Ishizuka N, et al., 1979 419 .


Figure 7. Muscle afferent projections in the rat spinal cord . Figure shows contour maps of varicosities from three afferents of each class (Group Ia, II, and Ib). Contour maps created by calculating the density of varicosities and outlining areas above a certain threshold. Approximate locations of spinal cord laminae are shown. Modified, with permission, from Vincent JA, et al., 2017 835 .


Figure 8. Task‐dependent modulation of somatosensory feedback . Effects of manually dorsiflexing the ankle (∼5°) during spontaneous (A) fictive locomotion and (B) fictive scratching in a decerebrate curarized cat. Figure shows activity from extensor and flexor nerves. EDL, extensor digitorum longus; MG, medial gastrocnemius; SmAB, semimembranosus‐anterior biceps; TA, tibialis anterior. Modified, with permission, from Frigon A and Gossard JP, 2010 282 .


Figure 9. Phase‐dependent modulation of cutaneous reflexes . Phase‐and speed‐dependent modulation of cutaneous reflexes evoked by electrically stimulating the superficial peroneal nerve (single 0.2 ms pulse at 1.2 times the motor threshold) in (A) semitendinosus, (B) vastus lateralis and (C) lateral gastrocnemius at a treadmill speed of 0.4 m/s in a spinal cat. Cutaneous reflexes are separated into 10 bins. Rectified EMG waveforms obtained with stimulation are separated into 10 bins (average of 5–17 cycles per bin). The black lines show the background level of EMG in each bin (average of ∼90 control cycles). The EMG waveform shown vertically on the right of each panel is the rectified activity of the muscle across the normalized cycle. Modified, with permission, from Hurteau MF, et al., 2017 407 .


Figure 10. Phase‐dependent modulation of postsynaptic potentials evoked by stimulating extensor and flexor muscle afferents at group I strength during fictive locomotion . (A) Nerves to plantaris (Pl) and sartorius (Srt) muscles were stimulated at group I strength during spontaneous fictive locomotion in a decerebrate curarized cat. Intracellular recordings from antidromically identified motoneurons were made with glass micropipettes filled with QX‐314. The type (i.e., inhibitory or excitatory) of last‐order interneuron activated within a given reflex pathway can be inferred by the sign of the postsynaptic potential recorded in the motoneuron. (B) During a fictive locomotor episode, the 2 nerves were stimulated with high frequency and short trains (6 pulses at 200 Hz) in alternation, with an interval of 150 to 250 ms between nerve stimulations. From top to bottom: Evoked responses tilted 90° evoked by Srt and Pl nerve stimulation given in alternation; intracellular membrane potential oscillations in the SmAB motoneuron showing the locomotor‐drive potential and superimposed evoked responses; ENGs from extensors, semimembranosus‐anterior biceps (SmAB), and lateral gastrocnemius‐soleus (LGS) and from a flexor, tibialis anterior (TA). The locomotor cycle was divided into extension and flexion phases according to the extensor ENG onset and offsets. (C) Postsynaptic potentials evoked by stimulating Srt and Pl nerves were divided and averaged into extension and flexion phases. Data were recorded in Jean‐Pierre Gossard's lab at the Université de Montréal.


Figure 11. Presynaptic inhibition through primary afferent depolarization . The figure shows synaptic contact between a primary afferent and a postsynaptic neuron. Two GABAergic interneurons make axo‐axonic contacts on the primary afferent. One GABAergic interneuron receives converging glutamatergic inputs from a group I afferent and from a CPG neuron while the other GABAergic interneuron receives input from a reticulospinal neuron. During locomotion, the group I afferent and CPG neuron depolarize their target GABAergic interneuron, leading to the release of GABA. GABA binds to GABA A ionotropic receptors on the primary afferent and opens Cl − channels. Cl − exits the primary afferent leading to a depolarization (PAD, primary afferent depolarization) and an electrotonic potential that travels in both directions. The antidromic PAD collides with the action potential coming from the periphery, reducing the orthodromic response and preventing release of glutamate at the primary afferent terminal. The electrotonic potential traveling in the orthodromic direction weakens in magnitude the further it travels and as it reaches the terminal, it is too weak to affect transmitter release.


Figure 12. Modulation of somatosensory feedback and its interactions with central locomotor networks . The figure shows potential mechanisms and interactions modulating inputs from a group Ib afferent of an ankle extensor. Upon entering the spinal cord, the Ib afferent makes synaptic contacts with neurons of the dorsal spinocerebellar tract (DSCT), the spinal locomotor CPG, represented as extensor and flexor half‐centers, as well as inhibitory and excitatory last‐order interneurons that project to ankle extensor motoneurons. The Ib afferent also ascends to brainstem nuclei that transmit the information to the cerebellum, thalamus, and cerebral cortex. At rest, the disynaptic inhibitory pathway is open and the excitatory pathway is inhibited. During locomotion, the spinal CPG inhibits the inhibitory pathway and releases the excitatory pathway from inhibition through disinhibition. At the same time, various supraspinal structures interact dynamically with each other and with spinal circuits, such as the spinal CPG and local reflex circuits.


Figure 13. Proprioceptive feedback and mouse genetics . (A) Selective removal of muscle spindles in Egr3‐KO mice occurs through loss of neurotrophin 3 (NT3) expression in the muscle spindles resulting in their degeneration postnatally. (B) Proprioceptive afferent neurons are selectively removed by making them selectively express the highly toxic DTA using the calcium‐binding protein Parvalbumin (Pv) and the transcription factor Isl2, both genes collectively expressed in proprioceptive afferents only. (C) Alternatively, proprioceptive afferent neurons can be made susceptible to the diphtheria toxin (DTX) by making them express the gene that encodes the diphtheria toxin receptor (DTR), normally not expressed in mice. In these mice, systemic injection of DTX results in acute removal of the proprioceptors. (D) The gene that encodes the DTR in a cre‐dependent manner can be postnatally delivered via adeno associated virus (AAV) injections into selected muscles. Later, as in (C), proprioceptive afferents only from the AAV injected muscles can be destroyed by systemic injection of DTX.


Figure 14. Hill‐type muscle model and its properties . (A) Three‐element Hill‐type model. CE, contractile element; PE, parallel elastic element; T, tendon; m, mass of muscle fascicles. (B) Normalized force‐length relationship of the contractile element fully activated and producing force isometrically, that is, without length change. Force is normalized to the maximum muscle force developed by the fully activated muscle at its optimal length. Length is normalized to the optimal muscle fascicle length. (C) Normalized force‐velocity relationship of the contractile element. Velocity is normalized to the maximum shortening velocity. Positive velocity corresponds to shortening. (D) Normalized tendon force‐length relationship. Parameters F Tnl , L Tnl and L T Max are empirical constants; L To is the resting (slack) tendon length. Adapted, with permission, from Prilutsky BI, et al., 2016 686 .


Figure 15. Pyridoxine intoxications reveal that large diameter somatosensory afferents contribute to postural control . (A) Schematic of the experimental set‐up. Filled circles represent kinematic markers. The antero‐posterior (AP) stance distance is the horizontal distance between the wrist and ankle joints. Forelimb, hindlimb, and trunk axis indicated by dashed lines. Reproduced and modified, with permission, from Fung J and Macpherson JM, 1999 293 . (B) Rectified averaged EMG activity of the gluteus medius and biceps femoris medial head before (control) and 7 days after pyridoxine intoxication, which destroys large‐diameter somatosensory afferents, in one cat with translation of the support surface at 240°. The dashed vertical line indicates the onset of platform acceleration. Under each trace, the arrows indicate response onset in control trials and at day 7. (C) Amplitude maximum initial displacement of the CoM and time of maximum displacement in relation to platform translation at 240°. Error bars indicate SE. **Significantly different from control values ( P  < 0.001, one‐way ANOVA). (B,C) Reproduced and modified, with permission, from Stapley PJ, et al., 2002 791 .


Figure 16. Somatosensory feedback is required for proper paw placement during skilled locomotion . (A) Cat stepping on a horizontal ladder before (control) and after a complete cutaneous denervation of the hindpaws. Based on, with permission, Bouyer LJ and Rossignol S, 2003 93 . (B) Egr3 mutant mice make more errors during walking on a horizontal ladder, determined as more frequent foot droppings between rungs than in wild types. Each bar indicates the number of steps that landed on a rung (black bars) or missed the rung (red bars) counted during one run. Each set of bar represents a run from different mouse ( n  = 13 for wild type and n  = 15 for Egr3 mutants). Based on, with permission, Akay T, et al., 2014 10 .


Figure 17. The loss of muscle spindle feedback in mice impairs swimming but not treadmill locomotion . Locomotor pattern gradually degrades with removal of proprioceptive feedback. (A) Chronic EMG recordings were made during treadmill locomotion and swimming in wild‐type and Egr3 mutants that lack functional muscle spindle feedback. (B) Bar diagram illustrating the activity of flexor (red) and extensor (blue) muscles during treadmill walking and swimming in wild‐type ( n  = 16 for walking and n  = 14 for swimming) and Egr3 mutant ( n  = 15 for walking and swimming) mice. Each horizontal bar is the average EMG activity in a normalized locomotor cycle (between successive swing or iliopsoas burst onsets for walking and swimming, respectively). GM, gluteus maximum; IP, iliopsoas; St, semitendinosus; TA, tibialis anterior; VL, vastus lateralis. Based on, with permission, Akay T, et al., 2014 10 .


Figure 18. Effect of stimulating muscle afferents during spontaneous fictive locomotion in decerebrate curarized cats . The figure shows the effect of stimulating the plantaris (Pl) nerve at group I strength and the sartorius (Srt) nerve at group II strength on the raw ENG bursts of activity during spontaneous fictive locomotion. Stimulation of the Pl nerve during (A) mid‐flexion resets the rhythm to extension while stimulation during (B) late extension prolongs the extensor burst. Stimulation of the Srt nerve during (C) early flexion resets the rhythm to extension while stimulation during (D) mid‐ to late extension has no visible effect. LGS, lateral gastrocnemius‐soleus; SmAB, semimembranosus‐anterior biceps; T, threshold; TA, tibialis anterior. Reproduced and modified, with permission, from Frigon A, et al., 2010 288 .


Figure 19. Proprioceptive feedback from extensor muscles contributes to the magnitude of extensor activity . (A) When the hindlimb of a decerebrate cat steps in a hole during treadmill locomotion, the EMG activity in ankle (LG, lateral gastrocnemius) and knee extensor (VM, vastus medialis) muscles is reduced. The shaded area indicates the time the foot entered the hole. (B) Loading ankle extensor muscles during foot‐in‐hole trials restored normal levels of EMG activity in ankle extensor muscles. The shaded area indicates the time the foot entered the hole without (top) and with (bottom) load applied to the Achilles tendon. Adapted, with permission, from Hiebert GW and Pearson KG, 1999 370 .


Figure 20. Cutaneous inputs regulate muscle activity and alter limb trajectory in a phase‐dependent manner . (A) The effects of stimulating the superficial radial (SR) and superficial peroneal (SP) nerves on the EMG activity of selected muscles and the phases of the four limbs during treadmill locomotion at 0.4 m/s in an intact cat. The SR and SP nerves were stimulated during mid‐stance and mid‐swing of the homonymous limb. The shaded area indicates the period of stimulation (25 pulses of 0.2 ms duration at 200 Hz and at 1.2 times the motor threshold). (B) Kinematic reconstruction of the forelimb (top panels) and hindlimb (bottom panels) without (control) and with stimulation during stance and swing. Note that in the top panels the left SR was stimulated while in the bottom panels the right SP was stimulated. Unpublished data from Frigon lab. BB, biceps brachii; ECU, extensor carpi ulnaris; FCU, flexor carpi ulnaris; GL, gastrocnemius lateralis; L, left; F, forelimb; H, hindlimb; R, right; Srt, anterior sartorius; ST, stance; TA, tibialis anterior; TRI, triceps brachii.


Figure 21. Cutaneous inputs regulate inter‐joint coordination during locomotion . The figure shows short‐latency pathways from cutaneous afferents of the superficial peroneal (SP) nerve to different hindlimb motoneurons during the flexion phase of fictive locomotion. The central pattern generator (CPG) is shown with mutually inhibiting extensor (E) and flexor (F) parts. The CPG can phasically modulate interneurons mediating di‐ and trisynaptic excitation of hindlimb motoneurons from SP afferents. The inhibitory pathway to ankle extensor motoneurons observed at rest (last‐order inhibitory interneuron In‐2) is inhibited by the spinal locomotor CPG. Ex‐1 and Ex‐2, excitatory interneurons 1 and 2; In‐1 and In‐2, inhibitory interneurons 1 and 2. Reproduced and modified, with permission, from Quevedo J, et al., 2000 705 .


Figure 22. Interlimb reflexes coordinate the four limbs during locomotion . Schematic of reflex pathways and main responses during stance and swing evoked by SP nerve stimulation. (A) Upon entering the spinal cord, primary afferents from the SP nerve contact (i) interneurons that project within the hemisegment (homonymous responses), (ii) commissural interneurons that project contralaterally (crossed responses), and (iii) ascending propriospinal neurons with their main axonal projections terminating ipsilaterally (homolateral responses) or on the other side (diagonal responses). Diagonal pathways cross at various segments along the length of the spinal cord and include collaterals from homolateral pathways that also project contralaterally. (B) Panels show the main pattern of forelimb and hindlimb responses evoked with SP nerve stimulation when the different limbs are in mid‐swing or mid‐stance. Responses shaded in dark blue represent excitatory responses while those in red represent inhibitory responses. Responses are aligned to the start of the stimulation. Adapted, with permission, from Hurteau MF, et al., 2018 408 .
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Article Title: Control of Mammalian Locomotion by Somatosensory Feedback
 

How to Cite

Alain Frigon, Turgay Akay, Boris I. Prilutsky. Control of Mammalian Locomotion by Somatosensory Feedback. Compr Physiol 2021, 12: 2877-2947. doi: 10.1002/cphy.c210020