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The Journal of Neurophysiology Vol. 79 No. 4 April 1998, pp. 1687-1701
Copyright ©1998 by the American Physiological Society
Department of Physiological Science, Laboratory of Neuromotor Control, University of California, Los Angeles, California 90095-1568
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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Carlson-Kuhta, Patricia, Tamara V. Trank, and Judith L. Smith. Forms of forward quadrupedal locomotion. II. A comparison of posture, hindlimb kinematics, and motor patterns for upslope and level walking. J. Neurophysiol. 79: 1687-1701, 1998. To gain insight into the neural mechanisms controlling different forms of quadrupedal walking of normal cats, data on postural orientation, hindlimb kinematics, and motor patterns of selected hindlimb muscles were assessed for four grades of upslope walking, from 25 to 100% (45° incline), and compared with similar data for level treadmill walking (0.6 m/s). Kinematic data for the hip, knee, ankle, and metatarsophalangeal joints were obtained from digitizing ciné film that was synchronized with electromyographic (EMG) records from 13 different hindlimb muscles. Cycle periods, the structure of the step cycle, and paw-contact sequences were similar at all grades and typical of lateral-sequence walking. Also, a few half-bound and transverse gallop steps were assessed from trials at the 100% grade; these steps had shorter cycle periods than the walking steps and less of the cycle (68 vs. 56%) was devoted to stance. Each cat assumed a crouched posture at the steeper grades of upslope walking and stride length decreased, whereas the overall position of the stride shifted caudally with respect to the hip joint. At the steeper grades, the range and duration of swing-related flexion increased at all joints, the stance-phase yield was absent at the knee and ankle joints, and the range of stance-phase extension at knee and ankle joints increased. Patterns of muscle activity for upslope and level walking were similar with some notable exceptions. At the steeper grades, the EMG activity of muscles with swing-related activity, such as the digit flexor muscle, the flexor digitorum longus (FDL), and the knee flexor muscle, the semitendinosus (ST), was prolonged and continued well into midswing. The EMG activity of stance-related muscles also increased in amplitude with grade, and three muscles not active during the stance phase of level walking had stance activity that increased in amplitude and duration at the steepest grades; these muscles were the ST, FDL, and extensor digitorum brevis. Overall the changes in posture, hindlimb kinematics, and the activity patterns of hindlimb muscles during upslope walking reflected the need to continually move the body mass forward and upward during stance and to ensure that the paw cleared the inclined slope during swing. The implications of these changes for the neural control of walking and expected changes in hindlimb kinetics for slope walking are discussed.
Examination of motor programs associated with stereotypic limb motions, including different forms of scratching in turtles (Mortin et al. 1985 Animal training and surgical procedures
Five laboratory-raised cats [Felis domesticus; 2 male (4.0-4.5 kg) and 3 female (3.0-4.2 kg)] were trained to walk at moderate speeds (0.6-0.7 m/s) on a motorized treadmill (0.3 × 0.8 m) enclosed with Plexiglas on all four sides. The same cats were also trained to walk up a walkway (1.85 × 0.29 m) with Plexiglas-sides (0.33 m) that led to a level platform (0.56 × 0.72 m). The walkway was inclined at one of four different grades: 25% (14° slope; Fig. 1A), 50% (26.6°; Fig. 1B), 75% (37°), and 100% (45°; Fig. 1C); many trials were recorded at each grade. The surface of the walkway and platform was covered with a thin, polyester, nonslip mat. During training sessions, sound, food, and affection were used to encourage continuous walking. Three animals (cats 2, 4, and 5) were also subjects for a previous study on crouched treadmill walking (Trank et al. 1996
Data collection, analyses, and statistics
Collection of EMG data has been described by Buford and Smith (1990) Step selection, cycle period data, and gait patterns
Data from cats 1-4 were used to determine the average cycle periods and hindlimb kinematics for upslope and level walking. Several trials at each grade were filmed, and during a single trial each cat typically completed 4-6 steps at its own speed to walk up the inclined walkway. Three criteria were used to select hindlimb steps from the film records for analysis: 1) steps were selected from trials in which the cats walked steadily up the walkway, with walking defined by Hildebrand's criteria (1976); 2) no steps were included in which the cats were moving onto or off the inclined walkway; and 3) cycle periods had to be within the range of 500-800 ms (consistent with moderate-speed walking) (see also Smith et al. 1993
Posture, hindlimb orientation, and stride length
Typical postures for level and upslope walking are illustrated in Fig. 1. During upslope walking, especially at the steeper slopes, the cats assumed a crouched posture with the trunk lowered and the head held forward, more in line with the trunk. Measurement of hip height from the walkway (Fig. 3, Hh) was used to assess the level of the hindquarter crouch. Hip height was similar at paw contact and liftoff for each step cycle, and average hip height decreased with increasing slope (Fig. 4). At the steepest grade hip height decreased on average by 29% from that of level walking. The difference in average hip height for walking at the 0 and 100% grades is illustrated in Fig. 3B.
Hindlimb kinematics for upslope walking
Exemplar kinematic data are illustrated in Fig. 5 for each of the four hindlimb joints. At all slopes, patterns of angular displacement were stereotypical and similar for all cats, and averaged records (such as those illustrated in Fig. 5) resembled kinematic records from individual steps. For each joint the average angular position at the step cycle transitions are listed in Table 2 and the average ranges of motion for each step cycle phase are given in Table 3.
SWING.
At the onset of swing, all joints were in flexion (F phase) to elevate the paw, and later in swing each joint extended (E1 phase) to lower the paw for contact (Fig. 5). Regardless of the grade, the reversal from F to E1 occurred first at the MTP joint and then at the knee, ankle, and hip joints, respectively (Table 1). From level walking to walking at the 25% grade, the percent of swing devoted to flexion increased at all joints except at the hip (Table 1). With steeper slopes, the percent of swing devoted to flexion increased at all joints and was highest at the 100% grade.
STANCE.
The hip, knee, and ankle joints were more flexed at paw contact with each increasing grade of upslope walking (Table 2, A-C), and these changes were consistent with the crouched posture. At the beginning of stance, the knee and ankle joints yielded (i.e., flexed; E2 phase) during level walking, and the yield was usually followed by a plateau during which there was little change in the angular position at either joint (Fig. 5, B and C). At the two lower grades the yield phase decreased in amplitude, and at the two steeper grades no yield occurred for 36 of 40 steps at the ankle joint and 18 of 40 steps at the knee joint (Table 3, B and C). When the knee joint did have a yield, the average value was only 3°.
INTRALIMB COORDINATION.
Changes in intralimb coordination for proximal and distal pairs of adjacent joints were assessed by angle-angle plots (e.g., cyclographs). The hip-knee cyclograms (Fig. 7A) illustrate a progression of changes over the five grades, from level (0% grade) to the 100% grade. The progressive shift of the five hip-knee plots toward the left-hand corner of the graph reflects the greater degree of flexion at both joints during slope walking, whereas the progressive increase in the size of the cyclograms reflects the increased range of motion at both joints, particularly during the swing-phase flexion and the stance-phase extension.
Motor patterns of selected hindlimb muscles during upslope walking
EMG data were collected from cats 1-5. Most muscles were examined for level walking and walking at all four upslope grades, but four distal muscles (FHL, FDB, EDL, and EDB) were recorded for level walking and walking at two grades, 25 and 75%. A total of 10-25 steps were analyzed for each cat at each grade of upslope walking. Typical averaged EMG traces, triggered to paw liftoff, are illustrated in Figs. 8 and 9 for proximal and distal muscles, respectively.
MUSCLES WITH STANCE-RELATED ACTIVITY ONLY.
Six muscles, each with extensor functions at the hip (ABF or ASM), knee (VL), or ankle (LG, PLT, or FHL) joints had only stance-related activity. The activity was initiated just before paw contact and continued for most of the stance at all grades. Although the timing of the extensor bursts was similar at all grades, the EMG amplitude increased at the steeper slopes (Figs. 8 and 9). For the VL burst, the profile of the rectified EMG signal was also slope related. The peak VL amplitude occurred soon after paw contact with level walking and at the lower grades. At the steeper slopes the peak was delayed until after midstance, and the amplitude increased gradually during the first half of stance (Fig. 8A).
MUSCLES WITH SWING-RELATED ACTIVITY ONLY.
Three muscles, each with a flexor function at the hip (IP) or ankle (TA or EDL) joints, had activity that was associated with swing-related motions. The IP and TA were active at the end of stance as the paw was being unweighted and continued to be active for most of the swing phase (Figs. 8 and 9). The EDL became active after paw liftoff and continued to be active during most of the swing phase. Although the timing of these swing-related EMG bursts was similar at all grades, the amplitude of the rectified, averaged EMG bursts increased with the grade of upslope walking. These increases are illustrated for the TA (Fig. 9), the EDL (Figs. 9 and 10), and, to a lesser extent, the IP (Fig. 8).
MUSCLES WITH STANCE- AND SWING-RELATED ACTIVITY.
Four muscles (FDB, FDL, EDB, and ST) had both stance- and swing-related activity during upslope walking, but EDB and ST stance-related activity was absent during level walking. Although the FDB had episodic activity during swing, the principal FDB activity occurred during stance and this activity increased substantially as the grade increased (Fig. 9). For level walking the FDL had a brief (24 ± 10 ms) swing-related burst that ended before liftoff. This burst increased in duration with increased slope, and at the 75% grade, FDL activity lasted an average of 123 ± 24 ms, extending well into swing (Figs. 9 and 10). Stance-related FDL activity was usually characterized by low-level EMG for level walking (Fig. 9A) and upslope walking at the 25% grade (Fig. 9B), but a distinct FDL burst usually occurred during the first third of stance at the 75% grade (Fig. 9C).
Half-bound and gallop steps at the steepest slope
The cats sometimes used half-bound and gallop steps to travel up the walkway at the steepest incline, and 11 of these trials were assessed for cats 1-4. Using Hildebrand's (1959, 1977) criteria, seven trials were classified as half-bound steps and four trials were classified as transverse gallop steps. The paw-contact sequence for one of the half-bound steps is shown in Fig. 2C. The hindlimbs acted together, whereas the forelimbs were slightly out of phase with each other. The same half-bound step is illustrated in Fig. 11A; here, cat drawings show the hindpaws lifting off and contacting the walkway together, although the left hindlimb was spatially ahead of the right hindlimb at the contact frame (Fig. 11A3). Also, the right forepaw was in stance before the hindpaws lifted off (Fig. 11A2); thus there was no free-flight period at the end of hindlimb stance. The absence of a free flight was typical for the half-bound and the gallop steps.
Slope-related changes in posture and hindlimb dynamics
During upslope walking the body mass must continually be moved forward and upward during stance, and the slope-related changes in posture and hindlimb kinematics were consistent with this need. For example, the caudal shift in the hindlimb stride at the steeper slopes is consistent with the need to increase the time for propulsion. During level walking, the hindpaw is placed well ahead of the hip joint at contact, and for about the first third of stance, the anterior-posterior shear component of the ground-reaction forces (GRF) provides a braking force (retropulsion) that resists the cat's forward motion; during the rest of stance, this shear component provides propulsion (Fowler et al. 1993 Motor pattern changes associated with upslope walking
There were two major pattern changes for upslope walking that were expected; e.g., increases in flexor activity during swing and increases in extensor activity during stance. In addition, there was one unexpected finding INCREASED FLEXOR ACTIVITY DURING SWING.
Increases in the amplitude and the duration of flexor activity during swing were related to increases in the range and duration of swing-phase flexion as the paw was elevated to greater heights to clear the inclined walkway. The changes were substantial for the FDL, a toe flexor, and the ST, a knee flexor. For the FDL, its swing-related burst increased in duration from 23 ms (level) to 124 ms (75% grade) as the range of toe flexion increased from 16 to 48° and the duration of flexion increased from 20 to 48% of swing, respectively. During crouched treadmill walking the FDL burst duration increased to an average of 90 ms and was associated with an increase in the range of MTP flexion but not in duration of swing-phase flexion (Trank et al. 1996 INCREASED EXTENSOR ACTIVITY DURING STANCE.
Muscles with extensor functions, particularly at the hip and ankle joints, as well as muscles with plantar-flexor functions (comparable with extensor) at the MTP joint, showed marked increases in EMG amplitude during upslope walking. These increases are consistent with measurements of increased muscle torques during stance of upslope walking. Fowler et al. (1993) ST ACTIVITY DURING STANCE.
The ST muscle was active during the first half of stance for upslope walking, and for two of four cats the ST had robust stance-related activity that increased with slope. The ST stance-related activity was unexpected because the ST is typically inactive during stance for level forward and backward walking (Buford and Smith 1990 Neuromotor control for upslope walking
Locomotion is thought to be controlled by a tripartite system that depends on central pattern generators (CPGs) at the spinal level, proprioceptive feedback from the moving limbs, and a variety of inputs from supraspinal centers (Grillner 1981 INCREASED EXCITATION LEVELS OF MOTONEURON POOLS.
One of the major changes for upslope walking is the need for increased excitation of specific flexor and extensor motoneuron pools. How are these increases in excitability affected? Similar increases in recruitment, particularly for extensor muscles, have been discussed with respect to speed-related changes in locomotion. As speed of locomotion increases, recruitment of motor pools increases, with small-tension producing motor units recruited before large-tension producing motor units according to Henneman's size principle (for review see Henneman and Mendell 1981 CHANGES IN THE STANCE SYNERGY.
Muscle synergies during locomotion are thought to be predetermined and controlled primarily by the interconnections of the CPG (Grillner 1981
POSTURAL CHANGES.
During upslope walking the level of the hindlimb crouch increased from the 50% grade to the 100% grade. At the steepest slope the crouched posture was similar to crouched treadmill walking elicited to mimic stalking (Trank et al. 1996
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
) and different forms of walking in crayfish and lobsters (Ayers and Davis 1977; Jamon and Clarac 1995), cats (Buford and Smith 1990; Smith andCarlson-Kuhta 1995; Trank et al. 1996), and humans (Thorstensson 1986; Winter et al. 1989) has contributed to the basic knowledge of the functions of skeletal muscles and yielded important insights regarding neural mechanisms for the control of limb motions. With regard to motor programs, these studies have shown that some aspects of the programs, all thought to be centrally generated, are common to more than one movement form, whereas other aspects are specific to a single task (see Stein and Smith 1997). Form-dependent details, such as muscle synergy groupings and the relative timing of individual muscle activities, are often associated with changes in body posture and limb orientation (Buford et al. 1990; Mortin et al. 1985; Smith and Carlson-Kuhta 1995; Trank et al. 1996), as well as the limb dynamics (Hoy and Zernicke 1985; Perell et al. 1993; Smith et al. 1993; Trank and Smith 1996; Winter et al. 1989).
; Halbertsma 1983; Walmsley et al. 1978). Later, research on hindlimb kinetics helped us understand motor pattern changes that were not easy to predict by knowledge of limb kinematics (Hoy and Zernicke 1985; Smith et al. 1993; Wisleder et al. 1990). For example, the knee joint flexes during the first part of the swing phase as the cat's paw is lifted up, and knee flexion increases in amplitude and velocity as the speed of locomotion increases (Wisleder et al. 1990). Not surprisingly, the electromyographic (EMG) activity (both duration and amplitude) of muscles with knee-flexor functions, such as the semitendinosus (ST), increases with speed. However, when the cat shifts from a trot to a gallop, even at the same treadmill speed, ST activity decreases abruptly even though the parameters of knee flexion are not altered (Smith et al. 1993). The marked decrease in ST activity during the gallop swing phase occurs because a flexor motion-dependent torque at the knee controls the joint action; thus muscle contraction is not required (Smith et al. 1993; Wisleder et al. 1990).
; Buford and Smith 1990; Perell et al. 1993; Pratt et al. 1996; Trank and Smith 1996), crouched walking (Trank et al. 1996), and upslope and downslope walking (Smith and Carlson-Kuhta 1995). For each walking form the cat's posture changes, there are important changes in the orientation of the hindlimb and several notable changes in the muscle synergies and recruitment of individual muscles. All of these changes are critical to the cat's abilities to adjust to the demands of the specific walking task.
; Herzog et al. 1993; Hoffer et al. 1989), or on changes in primate gait and hindlimb kinematics for walking at modest inclines (Vilensky et al. 1994). We know little about any adjustments in posture that might occur, alterations in hindlimb orientation that might be slope related, or changes in motor output that might be characteristic of upslope walking.
, 1996; Trank and Smith 1995) and in one rapid publication (Smith and Carlson-Kuhta 1995).
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
); cats have the same subject ID in both studies.
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FIG. 1.
Comparison of postures for level and upslope walking at 3 grades. Posture drawings for cat 1 were traced from the 1st paw-contact frame of the stance phase for the reference hindlimb (rH; here, the right hindlimb). For each pair of tracings, the unshaded drawing for upslope walking was superimposed over the shaded figure for level walking by aligning the measurement line for hip height, a line drawn from the hip joint marker perpendicular to the walkway surface (see Hh in Fig. 3A).
and Trank and Smith (1996). Briefly, three preanesthetic agents, atropine sulfate (0.05 mg/kg, im), acepromazine maelate (0.2 mg/kg, im), and ketamine hydrochloride (0.3 mg/kg, im) were administered before induction of pentobarbital sodium anesthesia (25 mg/kg, iv). During surgery pairs of Teflon-coated, multistranded, stainless steel wires (38 gauge) were implanted in selected hindlimb muscles, and the electrode wires were drawn subcutaneously to a multipin connector mounted to the skull. Cats 1-4 had hip and knee muscles implanted and cats 3-5 had ankle and digit muscles implanted.
for implant details)], flexor hallucis longus (FHL, ankle extensor and digit flexor; 1 cat), flexor digitorum brevis (FDB, digit flexor; 1 cat), and extensor digitorum brevis (EDB, digit extensor; 1 cat).
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TABLE 1.
Cycle period measurements for the reference hindlimb
and Trank and Smith (1996). EMG signals were usually amplified with a gain of 1,000, filtered (high pass at 100 Hz), and recorded onto FM tape (9.52 cm/s) with a binary code for data access. A computer program digitally converted the EMG signal off-line at a sampling rate of 1 kHz and stored it on disk. The signal was rectified and the bursts were analyzed with application software that determined burst onset and offset times by applying user-determined criteria for amplitude threshold. Because the automated analysis was impractical for some data because of multibursting activity, those bursts were chosen visually with the aid of a program-supplied cursor.
for the hip, knee, and ankle joints and by Trank and Smith (1996) for the metatarsophalangeal (MTP) joint. Briefly, a high-speed 16-mm ciné camera set at 100 frames/s was placed orthogonal to the treadmill or to the walkway to film the cat's locomotion. Rectangular coordinates of circular markers, glued on to the skin over joint centers and bony landmarks (see Fig. 1), were digitized from serial film frames with the use of an overhead projection system interfaced with a computer. The position of the knee joint was calculated by triangulation (Buford and Smith 1990). Smoothing filter frequencies were determined individually for each coordinate to maintain a root mean square error of 
0.05 mm. Linear and angular displacements were calculated from the filtered values. Step cycle phases for the hip, knee, and ankle joints were identified according to Philippson (1905) and Trank and Smith (1996; also see Kuhtz-Buschbeck et al. 1994) for the MTP joint.
). A Newman-Keuls posthoc test was used to test differences between cell means. Statements indicating a quantitative difference between data sets are based on a significance level of P 0.01.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
) to reduce the possibility that speed-related differences would be confounded with slope-related differences.
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FIG. 2.
Exemplar gait diagrams for 3 individual steps from cat 4. Each diagram is referenced to the step cycle of the rH (hindlimb facing camera); other limbs are contralateral hindlimb (cH), forelimb ipsilateral to rH (iF), and contralateral forelimb (cF). Bars represent stance period of each limb. A and B: lateral sequence gait; C: half-bound gait.
a tripod (rH-iF-cF)did not occur and the support provided by a diagonal couplet (rH-cF) was prolonged.
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FIG. 3.
Measurements of hindlimb orientation and stride length. A: measurements for cat 1 at the 50% grade are illustrated for paw contact. 
, anterior iliac crest (C), hip joint (H), knee joint (K), ankle joint (A), metatarsophalangeal (MTP) joint of 5th digit (M), and distal phalanx of 4th digit (D). - - -, segment lines represent the pelvis (C-H), thigh (H-K), shank (K-A), paw (A-M), and digits (M-D). Limb orientation measurements at paw contact (PC) are leg axis (LXa; H-D) and hip height (Hh), perpendicular distance from walkway to H; Da, distance from the Hh line to D, parallel to the walkway; and limb axis angle (Øa) at paw contact. B: limb orientation measurements at 0 and 100% grades are compared; data are 5 steps averaged at each grade for cat 2. PC and paw liftoff (PO) measurements are distinguished by ending with the letters "a" (anterior orientation) and "p" (posterior orientation), respectively. Calibration bars are 1 cm.
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FIG. 4.
Changes in hindlimb orientation measurements at paw contact (PC) and liftoff (PO) for slope walking; see Fig. 3 for abbreviations. Hh values were the same at PC and PO and the graph shows overlapping data points. Paw-liftoff measurements ( 
, 
, 
) and paw-contact measurements (
, 
, 
, 
) labeled as in Fig. 3. Each data point represents the average of 20 steps (5 per cat); all data were normalized and expressed as a percentage of the value for level walking (0% grade; - - -, 100%). Data points to the right under the G/HB heading are the same data points for gallop and half-bound steps at the steepest incline (100% grade).
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FIG. 5.
Typical hindlimb kinematics for level (0% grade) and upslope walking for hip (A), knee (B), ankle (C), and MTP (D). A and D: trace for the 50% grade was omitted because it was similar to the data trace for the 100% grade. - - -, SD lines based on 5 steps for each trace (cat 3; SD). Graphs begin and end with paw liftoff; , average time of paw contact.
View this table:
TABLE 2.
Angular positions of four hindlimb joints at step cycle transitions
View this table:
TABLE 3.
Ranges of motion during phases of the step cycle
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FIG. 6.
Slope-related changes in the range of motion at each hindlimb joint for the extension phase (E3) of stance. The height of bars represents the average range of motion at each grade; SD in Table 3. Significant stair-step increases in E3 extension occurred at the knee and ankle joints only. Unshaded bars mark 0, 50, and 100% grades; shaded bars mark 25 and 75% grades. Data based on 20 steps at each grade (5 steps/cat).
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FIG. 7.
Interjoint coordination for level (0% grade) and upslope walking. Angle-angle plots for hip-knee coordination (A) and ankle-MTP coordination (B) are the averages from 5 steps at each grade for cat 1. For each cyclograph, the step cycle starts and ends with PO and reads in a counterclockwise direction ( 
); paw contact is marked PC. Data points are plotted for each frame (10-ms intervals). *, knee plateau phase during stance that is typical of level walking (see text).
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FIG. 8.
A composite of average electromyographic (EMG) records from proximal muscles. Windows of data were triggered from PO (|) and then averaged over 6-13 steps. EMG records with similar cycle periods were selected; the average cycle periods were 779 ± 71 ms for level treadmill walking (0.5-0.6 m/s), 700 ± 19 ms for the 50% grade, and 612 ± 34 ms for the 100% grade. 
, estimated times for PC. The semitendinosus (ST), anterior biceps femoris (ABF), lateral gastrocnemius (LG), and tibialis anterior (TA) data are from cat 1 and the iliopsoas (IP), rectus femoris (RF), anterior semimembranosus (ASM), and vastus lateralis (VL) data are from cat 3. For each muscle, voltage calibration bars marked on the right side are the same for all records (A-C): VL (0.3 mV), RF and LG (0.2 mV), ABF (0.15 mV), IP and ST (0.1 mV), and ASM (0.075 mV). Horizontal timescale, 100-ms intervals.
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FIG. 9.
A composite of average EMG records from distal muscles. Windows of data were triggered from PO (|) and then averaged over 16-26 steps. EMG records with similar cycle periods were selected; average cycle periods were 711 ± 12 ms for level treadmill walking (0.5-0.6 m/s), 669 ± 69 ms for 25% grade, and 678 ± 21 ms for the 75% grade. - - -, estimated times for PC. Flexor hallucis longus (FHL), extensor digitorum longus (EDL), and TA data are from cat 3; flexor digitorum longus (FDL), plantaris (PLT), flexor digitorum brevis (FDB), and extensor digitorum brevis (EDB) data were from cat 5. For each muscle, voltage calibration bars marked on the right side are the same for all records (A-C): PLT (0.5 mV), FHL (0.25 mV), and FDL, FDB, EDB, EDL, and TA (0.125 mV). Horizontal timescale, 100-ms intervals.
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FIG. 10.
EMG records of single step cycles for level and upslope walking (cat 4) showing the prominent stance-phase ST burst at 2 upslope grades [50% (B) and 100% (C); 0% (A)]. , paw contact; |, paw liftoff. For each muscle, voltage calibration is the same for all muscles (0.25 mV) except for FDL (0.5 mV). Horizontal timescale, 100-ms intervals.
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FIG. 11.
Data for half-bound steps at the 100% grade. A: drawings from individual film frames show cat 4 at 3 different phases of the step cycle; A1) E2-E3 transition for the knee joint, A2) simultaneous liftoff of both hindpaws, and A3) simultaneous contact of both hindpaws. Hindlimb kinematics (B) for the hip (H), knee (K), and ankle (A) joints are shown for individual step cycles; trace begins at PC and ends with PO of the next step. EMG data for 4 muscles are synchronized in C with the hindlimb kinematics. * Lack of STpo burst after PO (see text). The gait diagram in Fig. 2C is also from this trial, and it begins with PC of the left hindlimb (onset of this record) and ends with PC at 3. |, ABF and TA (0.25 mV), ST and PLT (0.5 mV). Horizontal timescale, 100-ms intervals.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
). The transition between the retropulsion and propulsion occurs when the hip joint moves forward over the weightbearinghindpaw. With the alignment of the hindpaw nearly under the hip joint at contact of upslope walking, the portion of stance devoted to propulsion would be increased whereas the portion devoted to retropulsion would be reduced or even eliminated.
compared the peak magnitude of the braking and propulsive GRFs for level walking and walking at a 12° incline (similar to our 25% grade) and reported that the peak braking force decreased from 2.6 to 0.6 N, whereas the peak propulsive force increased from 2.8 to 6.1 N. Preliminary data from Smith et al. (1997) and unpublished data (R. Gregor) on the stance-phase kinetics of one medium-sized cat walking upslope at grades of 50 and 75% showed no braking force at the onset of stance, and the magnitude of the peak propulsive forces at midstance were as high as 13 N at the 75% grade.
). Although the level of hindquarter crouch was similar for both walking forms, the orientation of the hindlimb at paw contact and liftoff was different for upslope walking and consistent with the needs of walking up an incline. For example, the anterior placement of the hindpaw at contact decreased 55% for upslope walking at the steepest grade (compared with level) but only by 23% for level crouched walking. Also, the posterior position of the hindpaw at the end of stance increased only 13% for crouched walking but increased by 42% for upslope walking at the steepest grade. The marked increase in the posterior extension of the hindpaw at the end of upslope stance was associated with an increased range in extension during E3, as well as an increased peak extension at the ankle and hip joints.
; Grillner and Rossignol 1978). During upslope walking at the steepest slope, the average hip joint extension was 147 ± 7°; thus stance continued for some time after the hip joint reached the putative threshold to initiate swing. As upslope stance continued past the threshold, hindlimb extensors continued to contract, and the hindlimb continued to bear weight; thus group I muscle afferents, particularly those sensing contractile tension, would have continued discharge. The continued discharge of the group I muscles afferents, particularly at the ankle joint, would facilitate extensor muscle contraction at all hindlimb joints regardless of the hip joint's angular position and thus would prolong stance (Duysens and Pearson 1980; Guertin et al. 1995; Whelan et al. 1995).
prominent ST activity during the first part of stance at the steeper slopes. Each of these changes is discussed briefly.
). For backward walking both the range and the duration of MTP swing-phase flexion increased but the FDL burst was absent altogether, because flexion was produced by a flexor gravitational torque and flexor motion-dependent torques at the MTP joint (Trank and Smith 1996).
) and treadmill trotting (Smith et al. 1993). In each case the range and duration of swing-phase flexion at the knee joint increased and were associated with an increase in the magnitude of the flexor muscle torque for the knee joint at the beginning of swing (see Hoy and Zernicke 1985; Smith and Zernicke 1987; Smith et al. 1993).
). Inverse dynamics calculations of knee-joint torques show that flexion during the gallop is controlled by a flexor motion-dependent (inertial) torque and an extensor muscle torque at the knee joint, which acts to slow the rate of flexion caused by inertial forces (Smith et al. 1993). During upslope galloping steps, the STpo was also diminished or absent (Fig. 11), suggesting that the swing-phase dynamics at the knee joint may be similar for level and upslope galloping steps.
compared muscle torques at the ankle joint for level and upslope walking and found that the peak extensor muscle torque increased by 63% for upslope walking at 12° (similar to the 25% grade). Also, three groups of investigators (Fowler et al. 1993; Herzog et al. 1993; Hoffer et al. 1989) compared tendon forces of individual ankle extensor muscles for cats during level and upslope walking at modest inclines of 10-12°. They found that the peak forces, measured by tendon transducers, increased for LG and PLT but not for the soleus (see also Smith et al. 1977; Walmsley et al. 1978). Also, increases in tendon forces were closely matched with increases in rectified EMG signals (Herzog et al. 1993).
reported that the peak extensor muscle torque at the hip joint increased from 0.2 Nm (25% grade) to 1.2 Nm (75% grade). These substantial increases are consistent with our findings of robust slope-related increases in the EMG amplitude for hip extensor muscles. Smith et al. (1997) also reported that a flexor muscle torque occurred at the knee joint during the first 40% of stance for upslope walking at 75% grade. The torque then became extensor, increased rapidly, and peaked just before paw liftoff. Our VL EMG data for upslope walking shows that the VL is active after paw contact (but not before) and that VL activity peaked late in stance rather than early in stance as it does for level walking. This profile is consistent with the preliminary muscle torque data at the knee joint.
; Halbertsma 1983) and trotting and galloping (Smith et al. 1993). Why, then, is the ST active during the stance phase of upslope walking?
). For example, speed-related increases in the amplitude of STpc activity are related to increases in the magnitude of both muscle torques at the end of swing for walking and trotting (Smith et al. 1993; Wisleder et al. 1990). For backward walking, robust ST activity at the onset of swing is associated with an extensor muscle torque at the hip joint and a flexor muscle torque at the knee joint (Perell et al. 1993). Thus the increased ST activity during the stance phase of upslope walking is likely to be associated with increases in both torques.
reported a grade-related flexor muscle torque at the knee joint during the first part of stance of upslope walking. At the 75% grade the flexor muscle torque at the knee joint lasted for nearly one-half of the stance phase before changing to an extensor muscle torque. Thus, during the first part of upslope stance at the steeper slopes, there is a flexor muscle torque at the knee and an extensor muscle torque at the hip joint, and our EMG data suggest that ST recruitment contributes to both. Similarly, the LG and PLT, which are also recruited during the first part of upslope stance, would contribute to the flexor muscle torque at the knee joint and the extensor muscle torque at the ankle joint.
). During vertical jumps, ST activity begins before ABF activity, and both muscles are coactive during the initial stages of the upward thrust. The temporal sequence of ST and ABF activity for vertical jumping (see Fig. 10 of Zajac 1985) is similar to the sequence we show for half-bound steps. Zajac suggested that the recruitment of ST "acts to keep the knee flexed in the beginning of the jump." The ST probably has a similar function during half-bound steps; that is, it contributes to a knee flexor muscle torque. In many ways, half-bounding steps by cats up a steep incline are more similar to vertical jumps than half-bounding steps over a level surface.
; Lundberg 1980; Pearson and Rossignol 1991; Rossignol 1996). In the behaving animal all three elements interact to optimize the desired behavior. Although the role of each has been studied by investigators with the use of reduced preparations (for review see Rossignol 1996), we still do not understand how the three systems interact to control different forms of locomotion.
). Increases in the general excitation of motoneurons in the pool depend on increases in the excitation of CPG units provided by input from descending tracts and by input from motion-dependent feedback, whereas sensory input alone is thought to be of critical importance in the control of burst duration (Jordan 1991; Koshland and Smith 1989; Stein and Smith 1997). Independent control of amplitude and duration is apparent during locomotion. For example, the ABF burst may have a fivefold increase in amplitude during the stance phase of upslope walking compared with level, but the burst duration will be similar if the cycle durations are similar. In contrast, the ABF burst may have a twofold decrease in duration at a fast walking speed versus a slow speed, but increases in amplitude may be minimal.
; Goslow et al. 1973). At faster speeds the range of the yield increases and more potential energy is stored to further enhance force production. Because the yield at the ankle joint was absent at the steeper grades of upslope walking, any advantage the stretch-shorten cycle afforded was lost except for the half-bound and gallop steps at the steepest slope.
). Our earlier work on different forms of locomotion suggested that, in general, basic flexor-extensor synergies were common to forward walking, crouched walking, and backward walking, as well as trotting and galloping (Buford and Smith 1990; Smith et al. 1993; Trank and Smith 1996; Trank et al. 1996). With a few exceptions in digit muscles (see Trank and Smith 1996), these synergist groups are invariant, although details of the motor patterns, including the exact timing and amplitude of individual bursts, often depend on the form of locomotion.
; Halbertsma 1983). But our ST EMG data for different locomotor forms demonstrate that the timing and phasing of ST activity is often form specific; these data are summarized in Fig. 12. During backward walking, for example, a single ST burst occupies most of swing (Buford and Smith 1990), but in other forms of walking, including level forward walking (Buford and Smith 1990), crouched walking (Trank et al. 1996), downslope walking (Smith et al. 1998), and trotting (Smith et al. 1993), the ST has two swing-related bursts. At fast speeds of galloping, the ST may have only one swing-related burst, which occurs just before paw contact (Smith et al. 1993). In contrast, the ST may have stance-related activity during upslope walking and galloping (see Fig. 10).
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FIG. 12.
ST activity patterns for different forms of cat locomotion. Swing-related (or "flexor") activity is illustrated by unshaded bars and the stance-related (or "extensor") activity is shown by shaded bars. For convenience, the step cycle phases (PO and PC) are represented as being the same relative duration for all walking forms. Data taken from Buford and Smith (1990) for forward and backward walking, Smith et al. (1993) for trot and level gallop (
3.0 m/s), and Smith et al. (1998) for downslope walking; see DISCUSSION for more details.
), flexor related (Grillner and Zangger 1979), or both (Grillner and Zangger 1979). These data from fictive locomotion studies and our data from normal locomotion suggest that either a multifunctional network exists or that there are different CPGs that are form specific.
).
proposed a different solution by suggesting that the motor pool of each bifunctional muscle receives commands from a flexor and an extensor half-center. The combined strength of the two inputs, influenced by afferent input, determines the phasing of the muscle's activity (see Fig. 10 in Perret and Cabelquen 1980). In this way the ST might have pure extensor activity as it does during some steps of upslope galloping, pure flexor activity as it does during backward walking, or some combination of the two, as it does during upslope walking.
). To stalk prey, the cat walks low to the ground to avoid being seen, whereas the cat walks low to the ground at the steeper grades of upslope walking to increase its ability to maximize propulsion. For both behaviors posture changes are critical. This posture change is also true of backward walking, as the cat crouches and ventroflexes its trunk to shift the center of mass to maximize retropulsion (Buford et al. 1990; Perell et al. 1993).
; Mori et al. 1989) but not from the motor cortex (Beloozerova and Sirota 1993). Although the crouched postures typical of upslope or backward walking do not stem from the same intent that motivates cats to stalk prey (Bernston et al. 1976; Hutchinson and Renfew 1966), setting the posture may rely on the same connections within the brain stem and diencephalic areas (for review see Trank et al. 1996).
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ACKNOWLEDGEMENTS |
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We thank S. Lauretz (Animal Health Technician) for assistance with surgery, animal care and training, and data collection, as well as S. Saywell for a kinematic analysis of the upslope gallop data and C. Chen for assistance with the figures. We are also grateful to M. Orosz for developing the computer software used to analyze the kinematic variables illustrated in Fig. 3 and to R. Gregor at Georgia Institute of Technology for helpful suggestions on the DISCUSSION section.
This research was supported by National Institute of Neurological Disorders and Stroke Grant NS-19864 to J. L. Smith and a University of California, Los Angeles, Presidential Dissertation Year Fellowship to T. V. Trank.
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FOOTNOTES |
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Address reprint requests to J. L. Smith.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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