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Neural Control of Stereotypic Limb Movements

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Abstract

The sections in this article are:

1 Kinematics and Muscle Activity
1.1 Hindlimb Locomotor Movements
1.2 Forelimb Locomotor Movements
1.3 Walking at Different Speeds, Slopes, and Directions
1.4 Interlimb Coordination
1.5 Other Stereotypic Movements
2 Stereotypic Movements in Spinal Animals
2.1 Stereotypic Movements after Complete Spinal Lesions
2.2 Stereotypic Movements after Partial Spinal Lesions
2.3 Pharmacology of Stereotypic Patterns
3 Central Generation of Stereotypic Patterns
3.1 Locomotion
3.2 Interneurons
3.3 Scratching and Paw Shake
3.4 Ontogeny of Stereotypic Movements
3.5 Central Pattern Generator(s)
4 Afferent Controls
4.1 Proprioceptive Control
4.2 Cutaneous Control
4.3 Mechanisms of Reflex Modulation
5 Supraspinal Control
5.1 Initiation of Locomotion
5.2 Posture and Corrections
6 Concluding Remarks
Figure 1. Figure 1.

Kinematic and synchronized EMG activity of locomotion in a chronically implanted cat walking on a treadmill at 0.4 m/s. A, The flexor and extensor EMGs rectified and filtered and aligned on paw contact (dotted line). The average cycle is repeated twice. St, semitendinosus; Srt, sartorius anterior; VL, vastus lateralis; GM, medial gastrocnemius; GL, lateral gastrocnemius. B, The angle plots are taken from ten successive cycles with the dotted envelope indicating 1 standard error. In the duty cycle, the downward arrow is aligned with the vertical dotted line to mark paw contact; the two upgoing arrows are two successive foot lifts; E1, E2, and E3 refer to the subdivisions of the swing and stance according to Philippson . C, One complete cycle is reconstructed as stick diagrams for swing and stance; arrows indicate the direction of movement. D, The trajectory of each marker is displayed during one step cycle. The calibration applies to both C and D.

Figure 2. Figure 2.

Bar diagram of the activity of the principal hindlimb muscles during trot aligned on paw contact (downward arrows) with corresponding toe‐off in the preceding and following cycles. The patterns of EMGs were obtained from various sources (by scanning typical records) or rearranged from published values and aligned on paw contact. The inaccuracy resulting from these manipulations was judged to be offset by the advantages of displaying the several recorded muscles in a single format. Names and abbreviations of muscles are given together with the source.

The sources are: [1] = ; [2] = ; [3] = (1); [4] = ; [5] = ; [6] = (spinal cat during walk); [7] =
Figure 3. Figure 3.

Same as Figure but for the forelimbs. In A, 20 cycles are averaged; in B, 6 cycles. These cycles are normal step cycles in between cycles where the cat steps over obstacles.

From T. Drew and B. Kably, unpublished observations
Figure 4. Figure 4.

Same as Figure , but for the forelimbs during walk.

The sources are: [1] = for the dog; [2] = ; [3] = ; [4] =
Figure 5. Figure 5.

Changes of the kinematics with walking speed of a normal intact cat walking on a treadmill [from ]. A, Adjustments in the step cycle with speed. The stride cycle duration (Tc; triangles), the support phase duration (Tsu; circles), and the swing phases duration (Tsw, squares) are plotted vs. the velocity of locomotion. B, Adjustments of the support (Tsu, circles) and swing (Tsw, squares) phase duration with the stride cycle duration (Tc). Each symbol represents one interval. The straight lines were fitted to the data. C, Adjustments of the phases of the ankle joint with the stride cycle duration. The duration of the flexion phase (TFan) and of the third extension phase (TE3an; triangles) are plotted. Each symbol represents one interval. The straight line was fitted to these data and to the data of the duration of the first (TE1an) and second (TE2an) extension phase (data points not drawn for sake of clarity). Data from one cat. D, Adjustment of the amplitude of the limb movements—the support length—with speed. The support lengths are plotted as circles. The horizontal positions of the toe with respect to the hip during the support phase are plotted as bars. The top and bottom of the bars indicate the toe position at touch‐down and lift‐off, respectively. The support lengths are calculated from these positions. Each symbol represents data from a single stride. Approximately coinciding symbols are omitted for the sake of clarity.

Figure 6. Figure 6.

Summary of muscles activities for cyclic scratching. For each muscle, the bar represents the average burst duration normalized to the TA cycle period. Standard deviation of onset and offset latencies for each burst duration are denoted by horizontal lines to the left and right of each bar, respectively. Flexor muscles are indicated by shaded bars and extensor muscles by unshaded bars. Number of cycles analyzed for each muscle is listed at the right.

Adapted from Kuhta and Smith with permission
Figure 7. Figure 7.

Muscle synergies during paw shaking. In A, EMG of hip (GM, BF), knee (VL, BF), and ankle (GL, TA) muscles are shown for the beginning of a nine‐cycle paw shake response with a mean cycle period of 86 ms. In B, activities of these muscles are related to hindlimb motions during steady‐state cycles.

Adapted from Smith et al.
Figure 8. Figure 8.

Intrathecal injection of clonidine in an adult cat spinalized 3 days before. A, In the control period just before injecting clonidine, there is practically no rhythmic movement on the treadmill set at 0.2 m/s. B, About 30 min after the injection of clonidine (single bolus of 100 μg/100 μl) through the intrathecal cannula whose tip was around L5. Both the kinematics and EMG recordings show a nice pattern of walking.

From Chau, Barbeau, and Rossignol, unpublished observations
Figure 9. Figure 9.

Comparison of discharges in various muscle and muscle nerves in the same cat in three different conditions. In A, Normal cat, chronically implanted with EMG electrodes [see Drew and Rossignol for details of implantation] walking on a motor‐driven treadmill at 0.4 m/s. B, The same cat 20 days after spinalization and training [see Barbeau and Rossignol for details of training]. C, Same cat, 37 days following spinalization; the cat was decerebrated anemically, paralyzed with gallamine triethiodide, and injected with 4‐aminopyridine and clonidine. Nerve recordings are made with polymer cuff electrodes .

Reproduced with permission from Rossignol et al.
Figure 10. Figure 10.

Peristimulus rasters ordered by step cycle phase showing EMGs recorded simultaneously in tibialis anterior (TA) and gastrocnemius medialis (GM) muscles in response to 93 stimuli of superficial peroneal nerve at 4 × threshold for the fastest conducting afferents. Time bar at bottom, 20 ms before and 50 ms after stimulus presentation (*); regions marked control (C), P1, P2, and N1 correspond to diagonally oriented traces at right edge of each raster in which data point represents the mean EMG value for the corresponding peristimulus period of adjacent EMG trace. Bars along the left diagonal edge indicate Philippson step cycle phases during which stimulus was presented. F, flexion; E1, swing phase extension; E2 3, stance. Small black triangles indicate footlift (upward) and footfall (downward). The traces bracketed by the bars have been averaged to produce the correspondingly labeled, filled plots at the top; traces near the transitions have been excluded (note gaps between bars) because of uncertainty in their exact phasing. Bars have been phase‐advanced slightly from Philippson phases because of EMG phase‐lead (note short bar including the last few traces at the end of the stance period at the bottom of the rasters, with the F bars at the top.

Figure and legend modified from Loeb
Figure 11. Figure 11.

Amplitude of the integrated responses as a function of the time of stimulus application in the normalized step cycle. The graphs are divided into the reflex effects on muscles of the shoulder (A and B), elbow (C and D), and wrist and digits (E and F). Note that the responses in each muscle are expressed as a percentage of the maximal response in that muscle, or for inhibitory responses, to the minimal value. The stippled bars above each graph show the normal activity of the muscles during more than 30 unstimulated step cycles aligned with respect to the onset of activity in Br. The small horizontal lines give the standard deviation of the average values of EMG activity. The average occurrence of foot contact and foot lift is also indicated under each graph. In this experiment, no short‐latency effects were evoked in Biceps (Bic), cleidobrachialis (C1D), or supraspinatus (Ssp).

Reproduced from Drew and Rossignol
Figure 12. Figure 12.

Presynaptic events during fictive locomotion. A, Schematic representation of experimental procedures. 1 and 2, Sartorius nerve and vastus lateralis nerve recorded with bipolar Ag/AgCl electrodes in paraffine oil. 3, Electrical stimulation at a high frequency (>700 Hz) of peripheral superficial peroneal (SP) or tibial posterior (TA) nerves enclosed in polymer cuff electrodes. 4, Proximal stump of a cut dorsal rootlet was recorded with a bipolar Ag/AgCl electrode for dorsal root potentials (DRPs) in paraffine oil. 5, Micropipette filled with K+ citrate inserted close to the dorsal rootlet's entrance in the cord, 0.5–1.0 mm deep. 6, DC recording of the action potentials evoked by the high‐frequency stimulation of 3. Note the short constant latency and the absence of prepotentials (two superimposed sweeps). 7, AC recordings (100 Hz–10 KHz) of the responses to natural stimuli applied to the receptive field. The SP unit represented here is responding with bursts of action potentials (truncated) to three successive light air puffs on hair located on the dorsal aspect of the foot. Amplitude calibration of 6 does not apply to 7. In B and C, intra‐axonal recordings of cutaneous primary afferents during fictive locomotion. From top to bottom: intra‐axonal recording of an SP primary afferent or TA primary afferent, DRP from an L7 dorsal rootlet, flexor (Srtn), and extensor (VLn). In C, the intra‐axonal signal is thicker than in B because of the bandwidth (0.1 Hz–10 KHz) used to record action potentials.

From Gossard, Cabelguen, and Rossignol
Figure 13. Figure 13.

An overview of the structures involved in the initiation of locomotion. This figure was largely inspired by Garcia‐Rill , Gelfand et al. , and Jordan . 5N, trigeminal nuclear complex; CPG, central pattern generator; DLF, dorsolateral funiculus; EN, entopeduncular nucleus; IC, inferior colliculus; MLR, mesencephalic locomotor region; MRF, medullary reticular formation; NA, nucleus accumbens; PMLS, pontomedullary locomotor strip; PPN, pedonculopontine nucleus; PRF, pontine reticular formation; SLR, subthalamic locomotor region; SN, substantia nigra; Str, striatum; Th, thalamus; VLF, ventrolateral funiculus.



Figure 1.

Kinematic and synchronized EMG activity of locomotion in a chronically implanted cat walking on a treadmill at 0.4 m/s. A, The flexor and extensor EMGs rectified and filtered and aligned on paw contact (dotted line). The average cycle is repeated twice. St, semitendinosus; Srt, sartorius anterior; VL, vastus lateralis; GM, medial gastrocnemius; GL, lateral gastrocnemius. B, The angle plots are taken from ten successive cycles with the dotted envelope indicating 1 standard error. In the duty cycle, the downward arrow is aligned with the vertical dotted line to mark paw contact; the two upgoing arrows are two successive foot lifts; E1, E2, and E3 refer to the subdivisions of the swing and stance according to Philippson . C, One complete cycle is reconstructed as stick diagrams for swing and stance; arrows indicate the direction of movement. D, The trajectory of each marker is displayed during one step cycle. The calibration applies to both C and D.



Figure 2.

Bar diagram of the activity of the principal hindlimb muscles during trot aligned on paw contact (downward arrows) with corresponding toe‐off in the preceding and following cycles. The patterns of EMGs were obtained from various sources (by scanning typical records) or rearranged from published values and aligned on paw contact. The inaccuracy resulting from these manipulations was judged to be offset by the advantages of displaying the several recorded muscles in a single format. Names and abbreviations of muscles are given together with the source.

The sources are: [1] = ; [2] = ; [3] = (1); [4] = ; [5] = ; [6] = (spinal cat during walk); [7] =


Figure 3.

Same as Figure but for the forelimbs. In A, 20 cycles are averaged; in B, 6 cycles. These cycles are normal step cycles in between cycles where the cat steps over obstacles.

From T. Drew and B. Kably, unpublished observations


Figure 4.

Same as Figure , but for the forelimbs during walk.

The sources are: [1] = for the dog; [2] = ; [3] = ; [4] =


Figure 5.

Changes of the kinematics with walking speed of a normal intact cat walking on a treadmill [from ]. A, Adjustments in the step cycle with speed. The stride cycle duration (Tc; triangles), the support phase duration (Tsu; circles), and the swing phases duration (Tsw, squares) are plotted vs. the velocity of locomotion. B, Adjustments of the support (Tsu, circles) and swing (Tsw, squares) phase duration with the stride cycle duration (Tc). Each symbol represents one interval. The straight lines were fitted to the data. C, Adjustments of the phases of the ankle joint with the stride cycle duration. The duration of the flexion phase (TFan) and of the third extension phase (TE3an; triangles) are plotted. Each symbol represents one interval. The straight line was fitted to these data and to the data of the duration of the first (TE1an) and second (TE2an) extension phase (data points not drawn for sake of clarity). Data from one cat. D, Adjustment of the amplitude of the limb movements—the support length—with speed. The support lengths are plotted as circles. The horizontal positions of the toe with respect to the hip during the support phase are plotted as bars. The top and bottom of the bars indicate the toe position at touch‐down and lift‐off, respectively. The support lengths are calculated from these positions. Each symbol represents data from a single stride. Approximately coinciding symbols are omitted for the sake of clarity.



Figure 6.

Summary of muscles activities for cyclic scratching. For each muscle, the bar represents the average burst duration normalized to the TA cycle period. Standard deviation of onset and offset latencies for each burst duration are denoted by horizontal lines to the left and right of each bar, respectively. Flexor muscles are indicated by shaded bars and extensor muscles by unshaded bars. Number of cycles analyzed for each muscle is listed at the right.

Adapted from Kuhta and Smith with permission


Figure 7.

Muscle synergies during paw shaking. In A, EMG of hip (GM, BF), knee (VL, BF), and ankle (GL, TA) muscles are shown for the beginning of a nine‐cycle paw shake response with a mean cycle period of 86 ms. In B, activities of these muscles are related to hindlimb motions during steady‐state cycles.

Adapted from Smith et al.


Figure 8.

Intrathecal injection of clonidine in an adult cat spinalized 3 days before. A, In the control period just before injecting clonidine, there is practically no rhythmic movement on the treadmill set at 0.2 m/s. B, About 30 min after the injection of clonidine (single bolus of 100 μg/100 μl) through the intrathecal cannula whose tip was around L5. Both the kinematics and EMG recordings show a nice pattern of walking.

From Chau, Barbeau, and Rossignol, unpublished observations


Figure 9.

Comparison of discharges in various muscle and muscle nerves in the same cat in three different conditions. In A, Normal cat, chronically implanted with EMG electrodes [see Drew and Rossignol for details of implantation] walking on a motor‐driven treadmill at 0.4 m/s. B, The same cat 20 days after spinalization and training [see Barbeau and Rossignol for details of training]. C, Same cat, 37 days following spinalization; the cat was decerebrated anemically, paralyzed with gallamine triethiodide, and injected with 4‐aminopyridine and clonidine. Nerve recordings are made with polymer cuff electrodes .

Reproduced with permission from Rossignol et al.


Figure 10.

Peristimulus rasters ordered by step cycle phase showing EMGs recorded simultaneously in tibialis anterior (TA) and gastrocnemius medialis (GM) muscles in response to 93 stimuli of superficial peroneal nerve at 4 × threshold for the fastest conducting afferents. Time bar at bottom, 20 ms before and 50 ms after stimulus presentation (*); regions marked control (C), P1, P2, and N1 correspond to diagonally oriented traces at right edge of each raster in which data point represents the mean EMG value for the corresponding peristimulus period of adjacent EMG trace. Bars along the left diagonal edge indicate Philippson step cycle phases during which stimulus was presented. F, flexion; E1, swing phase extension; E2 3, stance. Small black triangles indicate footlift (upward) and footfall (downward). The traces bracketed by the bars have been averaged to produce the correspondingly labeled, filled plots at the top; traces near the transitions have been excluded (note gaps between bars) because of uncertainty in their exact phasing. Bars have been phase‐advanced slightly from Philippson phases because of EMG phase‐lead (note short bar including the last few traces at the end of the stance period at the bottom of the rasters, with the F bars at the top.

Figure and legend modified from Loeb


Figure 11.

Amplitude of the integrated responses as a function of the time of stimulus application in the normalized step cycle. The graphs are divided into the reflex effects on muscles of the shoulder (A and B), elbow (C and D), and wrist and digits (E and F). Note that the responses in each muscle are expressed as a percentage of the maximal response in that muscle, or for inhibitory responses, to the minimal value. The stippled bars above each graph show the normal activity of the muscles during more than 30 unstimulated step cycles aligned with respect to the onset of activity in Br. The small horizontal lines give the standard deviation of the average values of EMG activity. The average occurrence of foot contact and foot lift is also indicated under each graph. In this experiment, no short‐latency effects were evoked in Biceps (Bic), cleidobrachialis (C1D), or supraspinatus (Ssp).

Reproduced from Drew and Rossignol


Figure 12.

Presynaptic events during fictive locomotion. A, Schematic representation of experimental procedures. 1 and 2, Sartorius nerve and vastus lateralis nerve recorded with bipolar Ag/AgCl electrodes in paraffine oil. 3, Electrical stimulation at a high frequency (>700 Hz) of peripheral superficial peroneal (SP) or tibial posterior (TA) nerves enclosed in polymer cuff electrodes. 4, Proximal stump of a cut dorsal rootlet was recorded with a bipolar Ag/AgCl electrode for dorsal root potentials (DRPs) in paraffine oil. 5, Micropipette filled with K+ citrate inserted close to the dorsal rootlet's entrance in the cord, 0.5–1.0 mm deep. 6, DC recording of the action potentials evoked by the high‐frequency stimulation of 3. Note the short constant latency and the absence of prepotentials (two superimposed sweeps). 7, AC recordings (100 Hz–10 KHz) of the responses to natural stimuli applied to the receptive field. The SP unit represented here is responding with bursts of action potentials (truncated) to three successive light air puffs on hair located on the dorsal aspect of the foot. Amplitude calibration of 6 does not apply to 7. In B and C, intra‐axonal recordings of cutaneous primary afferents during fictive locomotion. From top to bottom: intra‐axonal recording of an SP primary afferent or TA primary afferent, DRP from an L7 dorsal rootlet, flexor (Srtn), and extensor (VLn). In C, the intra‐axonal signal is thicker than in B because of the bandwidth (0.1 Hz–10 KHz) used to record action potentials.

From Gossard, Cabelguen, and Rossignol


Figure 13.

An overview of the structures involved in the initiation of locomotion. This figure was largely inspired by Garcia‐Rill , Gelfand et al. , and Jordan . 5N, trigeminal nuclear complex; CPG, central pattern generator; DLF, dorsolateral funiculus; EN, entopeduncular nucleus; IC, inferior colliculus; MLR, mesencephalic locomotor region; MRF, medullary reticular formation; NA, nucleus accumbens; PMLS, pontomedullary locomotor strip; PPN, pedonculopontine nucleus; PRF, pontine reticular formation; SLR, subthalamic locomotor region; SN, substantia nigra; Str, striatum; Th, thalamus; VLF, ventrolateral funiculus.

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Serge Rossignol. Neural Control of Stereotypic Limb Movements. Compr Physiol 2011, Supplement 29: Handbook of Physiology, Exercise: Regulation and Integration of Multiple Systems: 173-216. First published in print 1996. doi: 10.1002/cphy.cp120105