Forms of Forward Quadrupedal Locomotion. III. A Comparison of Posture, Hindlimb Kinematics, and Motor Patterns for Downslope and Level Walking

Judith L. Smith, Patricia Carlson-Kuhta, and Tamara V. Trank

Department of Physiological Science, Laboratory of Neuromotor Control, University of California, Los Angeles, California 90095-1568

    ABSTRACT
Abstract
Introduction
Methods
Results
Discussion
References

Smith, Judith L., Patricia Carlson-Kuhta, and Tamara V. Trank. Forms of forward quadrupedal locomotion. III. A comparison of posture, hindlimb kinematics, and motor patterns for downslope and level walking. J. Neurophysiol. 79: 1702-1716, 1998. To gain further insight into the neural mechanisms for different forms of quadrupedal walking, data on postural orientation, hindlimb kinematics, and motor patterns were assessed for four grades of downslope walking, from 25% (14° slope) to 100% (45°), and compared with data from level and downslope walking at five grades (5-25%) on the treadmill (0.6 m/s). Kinematic data were obtained by digitizing ciné film, and electromyograms (EMGs) synchronized with kinematic records were taken from 13 different hindlimb muscles. At grades from 25 to 75%, cycle periods were similar, but at the steepest grade the cycle was shorter because of a reduced stance phase. Paw-contact sequences at all grades were consistent with lateral-sequence walking, but pace walking often occurred at the steepest grades. The cats crouched at the steeper grades, and crouching was associated with changes in fore- and hindlimb orientation that were consistent with increasing braking forces and decreasing propulsive forces during stance. The average ranges of motion at the hindlimb joints, except at the hip, were often different at the two steepest slopes. During swing, the range of knee- and ankle-joint flexion decreased, and the range and duration of extension increased at the ankle joint to lower the paw downward for contact. During stance the range of flexion during yield increased at the ankle joint, and the range of extension decreased at the knee and metatarsophalangeal joints. Downslope walking was also associated with EMG changes for several muscles. The hip extensors were not active during stance; instead, hip flexors were active, presumably to slow the rate of hip extension. Although ankle extensors were active during stance, their burst durations were truncated and centered around paw contact. Ankle flexors were active after midstance at the steeper slopes before the need to initiate swing, whereas flexor and extensor digit muscles were coactive throughout stance. Overall the changes in posture, hindlimb kinematics, and activity patterns of hindlimb muscles during stance reflected a need to counteract external forces that would accelerate angular displacements at some joints. Implications of these changes are discussed by using current models for the neural control of walking.

    INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References

The assessment of quadrupedal walking forms in the cat has proven to be an inexhaustible area to study the different functions of skeletal muscles in the production of limb motion and to gain insight into the neural mechanisms required for locomotor control. Accounts of these studies are provided in the INTRODUCTION of companion papers to this study (Carlson-Kuhta et al. 1998; Trank et al. 1996), as well as in recent reviews focused on the neural control of locomotion (Rossignol 1996; Stein and Smith 1997) and limb dynamics (Zernicke and Smith 1996). Here we detail the changes in posture, hindlimb orientation, and kinematics, as well as the motor patterns of selected hindlimb muscles associated with downslope walking at grades from 5 to 100%. These data are compared with similar data for upslope walking (Carlson-Kuhta et al. 1998) and crouched walking (Trank et al. 1996), as well as forward and backward walking on a level surface (Buford and Smith 1990; Buford et al. 1990; Perell et al. 1993; Pratt et al. 1996; Trank and Smith 1996).

Our data for downslope walking suggest that adjustments in postural orientation and hindlimb kinematics occur to reduce the propulsive phase of stance and at the same time serve to increase the braking forces associated with stance, especially at the steeper slopes. These adjustments require major changes in the activity patterns of specific hindlimb muscles, particularly the flexor and extensor muscles of the hip joint during the stance phase. These motor pattern changes, unique to downslope walking, are discussed in terms of current models for the neural control of locomotion. Preliminary results of our studies on downslope walking were published in four abstracts (Carlson-Kuhta and Smith 1995; Smith et al. 1994, 1996; Trank and Smith 1995) and in one rapid publication (Smith and Carlson-Kuhta 1995).

    METHODS
Abstract
Introduction
Methods
Results
Discussion
References

Except where noted, the methods were identical to those described in the study of upslope walking in the companion paper (Carlson-Kuhta et al. 1998). Six laboratory-raised cats [Felis domesticus; 4 male (4.0-4.5 kg) and 2 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. Four of these cats (1 and 3-5) were also subjects for the upslope study in the companion paper (same identification numbers). The cats were also trained to walk down a walkway (1.85 × 0.29 m) with Plexiglas sides (0.33 m) from an elevated level platform (0.56 × 0.72 m). The walkway was inclined at one of four different grades: 25% (14° incline; Fig. 1A), 50% (26.6°; Fig. 1B), 75% (37°), and 100% (45°; Fig. 1C).


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FIG. 1. Comparison of postures for level and downslope walking at 3 grades [25% (A), 50% (B), and 100% (C).] Posture drawings for cat 5 were traced from the first paw-contact frame of the reference hindlimb (rH; here, the left hindlimb). For each pair of tracings, the unshaded drawing for downslope walking was superimposed over the shaded figure for level walking by aligning the measurement line for Hh, a line drawn from the hip-joint marker perpendicular to the walkway surface (also see Hh in Fig. 3A).

Electromyographic (EMG) data was recorded from 13 different hindlimb muscles, and typically each cat had 4-6 muscles implanted: anterior biceps femoris (ABF, hip extensor; 3 cats), anterior semimembranosus (ASM, hip extensor; 1 cat), iliopsoas (IP, hip flexor; 1 cat), semitendinosus (ST, hip extensor and knee flexor; 3 cats), rectus femoris (RF, hip flexor and knee extensor; 2 cats), vastus lateralis (VL; knee extensor; 2 cats), lateral gastrocnemius (LG, knee flexor, ankle extensor; 1 cat), tibialis anterior (TA, ankle flexor; 3 cats), extensor digitorum longus (EDL, digit extensor and ankle flexor; 2 cats), plantaris (PLT, ankle extensor and digit flexor; 2 cats), flexor digitorum longus (FDL, digit flexor; 2 cats), 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).

Cats 6 and 7 were trained to walk downslope on the same treadmill used to test level walking. For downslope trials the back of the treadmill was elevated on a custom-designed wooden ramp that could be altered to change the incline of the treadmill. Each cat was tested and filmed at five different grades [5% (3° slope), 10% (6°), 15% (8.5°), 20% (11°), and 25% (14°)] at a moderate walking speed of 0.6 m/s. Muscles recorded from cats 6 and 7 included the IP, ABF, and VL; in addition, the ASM was recorded from cat 6 and the RF was recorded from cat 7.

To compare various kinematic and EMG parameters for level and downslope walking on the walkway, a repeated measures analysis of variance (ANOVA) was used (Altman 1991). A Newman-Keuls posthoc test was used to test differences between cell means. All statements that indicate a quantitative difference between data sets are based on a significance level of P <=  0.05.

    RESULTS
Abstract
Introduction
Methods
Results
Discussion
References

Cycle period data and gait patterns: grades 25-100%

Data from four cats (cats 1 and 3-5) were used to determine the average cycle periods and hindlimb kinematics for overground, downslope walking. Several trials at each grade (25-100%) were filmed for each cat (Fig. 1). During a single trial each cat usually completed 5-6 steps, walking at its own speed down the walkway. Criteria used to select individual hindlimb steps from the film records are described in Carlson-Kuhta et al. (1998). The five best walking steps were analyzed for each cat at each grade; thus a total of 80 steps were assessed. The downslope data were compared with data from level treadmill walking (5 steps per cat).

Cycle periods for the reference hindlimb (rH; e.g., the one facing the camera) were measured from successive paw liftoffs and averaged across cats for each grade. The average cycle period and percent of cycle devoted to stance were similar for downslope walking at grades of 25, 50, and 75% (Table 1). The average cycle periods at these grades were shorter than the average cycle periods for level treadmill walking at 0.6 m/s, but the structure of the step cycle was similar, with an average of 62-68% of the cycle devoted to stance. These data are consistent with Hildebrand's (1976) definition of "moderate" walking. The average cycle period at the steepest grade was shorter than those for the walking steps at all other grades; also the percent of cycle devoted to stance was typically <60% (Table 1). The data for slope walking at the 100% grade are within Hildebrand's (1976) range of a "fast" rather than a moderate walk.

 
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TABLE 1. Cycle period measurements for the reference hindlimb

Gait diagrams were constructed for each step according to Hildebrand's (1976) criteria. As illustrated by the four exemplar gait diagrams in Fig. 2, the sequence of paw-contact patterns was the same at all grades of downslope walking. Specifically, contact of the reference hindpaw (labeled rH) was followed by contact of the ipsilateral forepaw (iF), contralateral hindpaw (cH), and then contralateral forepaw (cF). Although the contact sequence of rH-iF-cH-cF, called the "lateral sequence" by Hildebrand (1976), was the same at all grades, the time intervals between contacts were variable, leading to a variety of support combinations during the gait cycle.


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FIG. 2. Gait diagrams for four individual steps [25% (A), 50% (B), 75% (C) and 100% (D)] from cat 1. Each diagram is referenced to the step cycle of the rH (the hindlimb facing the camera). Bars represent the stance phase for each limb. cH, contralateral hindlimb; iF, forelimb ipsilateral to rH; and cF, contralateral forelimb.

The gait diagrams in Fig. 2 are characterized by combinations of tripod and biped support. For example, Fig. 2B shows the eight support combinations typical of lateral sequence walking: 1) rH-cH-cF (tripod support; also see Fig. 1, A-C); 2) rH-cF (diagonal couplet); 3) rH-iF-cF (tripod); 4) rH-iF (lateral couplet); 5) rH-iF-cH (tripod); 6) iF-cH (diagonal couplet); 7) iF-cH-cF (tripod); and 8) cH-cF (lateral couplet). The same sequences are illustrated in Fig. 2D, but the duration of the eight combinations was not equal; for example, the third tripod support was very brief, whereas the second diagonal couplet was prolonged.

The support sequences in Fig. 2, A (25% grade) and C (75% grade), show periods of tetrapod support in addition to periods of biped and tripod support. In Fig. 2A, for example, the iF made contact before cH was lifted (~15% of the rH cycle); consequently, there was a brief period of tetrapod support. Another brief period of tetrapod support occurred after the cF made contact before the rH was lifted up (~60% cycle). Two similar periods of tetrapod support are shown in Fig. 2C.

In the gait diagram of Fig. 2C, the predominant support pattern is provided by lateral couplets, first rH-iF and then cH-cF. These support patterns are characteristic of pace walking (Hildebrand 1976). Pace walking tended to be more common at the two steeper grades, and this tendency is illustrated in Fig. 1. At the 25% grade (Fig. 1A), the left hindpaw made contact just after the left forepaw lifted off, and the hind- and forepaw are spatially very close; this is typical of a lateral sequence walk. At the steeper grades the spatial distance between the two ipsilateral paws often increased as forepaw contact occurred soon after the hindpaw made contact (Fig. 1C); this is typical of pace walking.

Posture, hindlimb orientation, and stride length: grades 25-100%

Typical postures for level and downslope walking are compared in Fig. 1. During downslope walking, particularly at the steeper grades, the cats assumed a crouched posture with the trunk lowered. We measured hip height from the walkway (Fig. 3A, Hh) at key points in the step cycle, and these measurements were used to assess the level of the hindquarter crouch. Hip height was similar at paw contact and liftoff, and average hip height decreased with increasing slope (Fig. 4, Hh). At the steepest slope, hip height decreased an average of 26% from that of level treadmill walking.


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FIG. 3. Measurements of hindlimb orientation and stride length. A: limb measurements for cat 4 at the 50% grade for paw liftoff. bullet , 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) - - -, line segments represent the pelvis (C-H), thigh (H-K), shank (K-A), paw (A-M), and digits (M-D). Limb orientation measurements at paw liftoff are LXp [leg axis (H-D)] and Hh [hip height] perpendicular distance from walkway to H; Dp, distance from Hh line to D, parallel to the walkway; and Øp, limb axis angle at paw liftoff. B: limb orientation measurements at 0 and 100% grades are compared; data are 5 steps averaged at each grade for cat 3. Paw contact (PC) and paw liftoff (PO) measurements are distinguished by the ending letters "a" (anterior orientation) and "p" (posterior orientation), respectively. Calibration bars, 1 cm.


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FIG. 4. Changes in hindlimb orientation measurements at paw contact and liftoff for downslope walking; see Fig. 3 for abbreviations. black-diamond , bullet , black-triangle, and black-square: paw liftoff measurements, labeled p (posterior orientation); diamond , square , triangle , and open circle : paw-contact measurements, labeled a (anterior orientation). Each data point represents the average of 20 steps (5 steps/cat); all data were normalized and expressed as a percentage of the value for level walking (- - -, 100%).

Decreases in hip height were associated with changes in hindlimb orientation at paw contact and liftoff, and measurements used to quantify the changes are illustrated and defined in Fig. 3. At paw contact the hindpaw was always placed anterior to the hip joint (Fig. 3, Da), and there was a modest increase in the anterior placement of the paw that was similar for all grades of downslope walking compared with level walking (Fig. 4). The length of the limb axis (Fig. 3, LXa) decreased as the angle of the limb axis (Fig. 3, Øa) increased at the steeper grades (Fig. 4). At paw liftoff the hindpaw was always posterior (caudal) to the hip joint, and the posterior distance (Fig. 4, Dp) decreased at the steeper grades. Also, there was a progressive decrease in the length of the limb axis (Fig. 3, LXp) and the angle of the limb axis (Fig. 3, Øp) at paw liftoff across the four grades of downslope walking (Fig. 4).

Total stride length, the distance from paw liftoff to contact (Fig. 3B, Dp + Da), was reduced for slope walking by 7-15% at the two lower slopes and by 30-40% at the two steeper slopes. Because Da was consistent at the steeper slopes, the overall decrease in stride length was due to the marked reduction in Dp (Fig. 4). A comparison of average stride lengths for walking steps at 0 and 100% grades is shown in Fig. 3B.

The posture illustrations in Fig. 1 also show changes in the orientation of the forelimbs and the entire trunk for downslope walking at the steep slopes. At the 100% grade, the forepaws were aligned under the chin (Fig. 1C) rather than under the base of the neck (Fig. 1A). Because the cats' bodies had been marked specifically to assess the effects of downslope walking on hindlimbs, we had no adequate means to quantify the apparent shift in forepaw position or the trunk's apparent downward slant at the two steeper grades.

Hindlimb kinematics: grades 25-100%

Kinematic data for each hindlimb joint are illustrated in Fig. 5. For level walking and walking at the 25% grade, the patterns of angular displacement were stereotypical and similar for all cats; thus averaged records, such as those illustrated in Fig. 5, resembled kinematic records from individual steps. At the steeper slopes, however, the kinematic data for the knee and ankle joints tended to be more variable from step to step for all cats, as indicated by wider than usual standard deviation bands for the knee-joint data in Fig. 5B (50 and 100% grades) and the ankle-joint data in Fig. 5C (50% grade). The tendency for greater variability at the steeper slopes is also indicated by the frequency of SD >10° in Table 2, which lists the angular positions of the hindlimb joints at key transitions of the step cycle, and Table 3, which lists the ranges of motion for the major phases of the step cycle.


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FIG. 5. Typical hindlimb kinematics for level (0% grade) and downslope walking. Graphs begin and end with paw liftoff; bullet , average time of paw contact. - - -, SD lines for downslope data, based on 5 steps for each trace (cat 3); see Fig. 5 in Carlson-Kuhta et al. (1998) for the SD bands of the level walking data.

 
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TABLE 2. Angular positions of the hindlimb joints at step cycle transitions

 
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TABLE 3. Ranges of motion during phases of the step cycle

SWING. At the onset of swing, the hip, knee, and ankle joints were more flexed at the steeper slopes (Table 2, PO) and this increased flexion was consistent with the crouched posture and the reduction in the length of the hindlimb axis at liftoff (Fig. 4, LXp). The range of hip-joint flexion at the beginning of swing was the same at all grades; however, the range of flexion decreased at the knee and ankle joints at the two steeper slopes (Table 3, B-C: F). In contrast, the range of flexion at the metatarsophalangeal (MTP) joint increased twofold from 0% to the 25% grade but increased no further at the steeper grades (Table 3D, F-swing).

Later in swing each joint extended (E1 phase) to lower the paw for contact. The reversal from F to E1 always occurred first at the MTP joint followed by the knee, ankle, and hip joints, in that order (Table 1). At the two proximal joints, the average ranges of swing-phase extension were similar at all grades. At the ankle joint, however, the average range of extension increased at the steepest slope (Table 3C, E1) compared with level walking, whereas the range of MTP extension increased at the 25% grade and increased again at the steepest slope (Table 3D, E1).

STANCE. At paw contact the hindlimb joints were more flexed at the steeper slopes (Table 2, PC); this was consistent with the crouched posture at the beginning of stance and the reduction in the length of the hindlimb axis (Fig. 4, LXa). As illustrated in Fig. 5, the hip and MTP joints extended throughout most of stance, whereas the knee and ankle joints flexed (yield or E2 phase) and then extended (E3 phase).

During the yield, the range of flexion at the ankle joint increased at the two steeper slopes (Table 3C, E2), whereas the range of knee-joint flexion during yield was similar for all grades of downslope walking. The MTP joint, which had no measurable yield during the stance phase of level walking (Fig. 5D), flexed around the time of paw contact at all downslope grades. As illustrated in Fig. 6, flexion at the MTP joint was initiated before paw contact and continued into the beginning of stance. Here, the MTP joint began to flex ~20 ms before paw contact, as the digits moved slightly downward to make an adjustment for contact. The MTP joint continued to flex after contact, as the tarsals were lowered toward the surface of the ramp during the initial weight-bearing phase. This flexion phase constituted a yield at the MTP joint not usually observed for level walking (but see Kuhtz-Buschbeck et al. 1994), and the range of flexion was usually small, ranging from 1 to 9°.


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FIG. 6. Flexion of the MTP joint around paw contact for downslope walking. Drawings taken from a single step at the 75% grade (cat 4); to reduce the vertical size of the illustration, the sloped walkway was reoriented to the horizontal. The 4 paw drawings were traced from alternate film frames (1 frame = 10.3 ms); 1 illustrates the plantar angle measured for the MTP. The numbered dots on the data trace correspond to the enumerated paw drawings. MTP flexion began before paw contact (PC) as the digits move downward and flexion continued into stance as the tarsals moved downward; also see text. The dashed horizontal line was added as a referent to the vertical motion of the ankle-joint dot.

Although the ranges of extension at the hip and ankle joints were similar for all grades of downslope walking, the ranges of extension at the knee and MTP joints were reduced at the steeper slopes (Table 3, B and D: E3). At the moment of peak extension during stance, all joints were less extended for downslope than level walking at the steeper slopes. The ankle joint, in particular, was less extended at successive grades (Table 2, Peak E).

Peak extension at the end of stance was followed by a brief period of flexion at all joints before paw liftoff (Fig. 5). The range of flexion at the hip, knee, and ankle joints was small (~3-5°), and neither the range of stance-phase flexion nor the timing of the extension-flexion reversal was related to the grade of downslope walking. The range of MTP flexion during stance was substantial for level walking (Fig. 5D) and did not change with downslope walking (Table 3D, F-stance).

INTRALIMB COORDINATION. Intralimb coordination for proximal and distal pairs of adjacent joints was assessed by angle-angle plots (e.g., cyclographs). The hip-knee cyclographs (Fig. 7, A-B) show a progression of grade-related changes. In Fig. 7A, the progressive shift to the left was due to the crouched posture and a greater degree of flexion at the knee joint, whereas the diagonal shift in Fig. 7B was due to a progressive increase in the flexed position at the hip and knee joints. In Fig. 7A, the plot for downslope walking at 50% also increased in the vertical and horizontal dimensions. These expansions demonstrate the increases in the ranges of hip-joint flexion and knee-joint extension during swing; both of these changes were typical of cat 1 but not of the other cats.


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FIG. 7. Interjoint coordination for level and downslope walking at 4 grades. Angle-angle plots in A and B (hip-knee coordination) and C and D (ankle-MTP coordination) are the averages from 5 steps for each grade. For all cyclographs, the step cycle starts and ends with paw liftoff (PO) and reads in a counterclockwise direction, as indicated by the arrows; paw contact is marked by the arrowheads labeled PC. Data points are plotted for each film frame (10-ms intervals). Data in A and C are from cat 1, B and D, cat 4.

The ankle-MTP cyclographs (Fig. 7, C-D) also show a progressive diagonal shift to the lower left that was due to an increase in the crouched (flexed) posture at the ankle and MTP joints. The horizontal expansions to the left (more typical of Fig. 7C than 7D) were due to an increased range of MTP joint flexion. Also, Fig. 7, C-D, illustrate a primary contour change that was slope related. Here, notice the progressive increase in the indentation that occurred around paw contact (Fig. 7C, arrowhead marked PC). The increased indentation was due to a greater range of ankle-joint E1 extension during swing and then a greater range of flexion during the stance yield at the steeper slopes. In some steps, as shown in Fig. 7D, the indentation became a loop when flexion at the MTP joint preceded paw contact as well as the onset of ankle flexion at the beginning of stance.

Motor patterns of hindlimb muscles: grades 25-100%

EMG data were collected from cats 1 and 3-5 during level walking on the treadmill and downslope walking on the inclined walkway. Most muscles were examined for level walking and at all four grades, but four distal muscles (FHL, FDB, EDL, and EDB) were recorded for level walking and only at two grades, 25 and 75%. For each muscle, 10-25 steps were typically analyzed for each grade. Exemplar averaged EMG traces, triggered to paw liftoff, are illustrated in Figs. 8 and 9 for proximal and distal muscles, respectively. For comparison purposes, the durations of the EMG bursts were normalized to the cycle period.


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FIG. 8. A composite of average electromyogram (EMG) records from proximal muscles. Windows of data were triggered from paw liftoff (|) and then averaged over 13-15 steps. EMG records with similar cycle periods were selected for each grade; average cycle periods were 779 ± 71 ms forlevel treadmill walking (0.5-0.6 m/s), 656 ±45 ms for 50% grade, and 442 ± 15 ms for the 100% grade. ⋮, estimated times for paw contact. The semitendinosus (ST), anterior biceps femoris (ABF), and lateral gastrocnemius (LG) data are from cat 1 and the iliopsoas (IP), rectus femoris (RF), anterior semimembranosus (ASM), and vastus lateralis (VL) data are from cat 3, with 10-15 steps averaged for each trace. Level walking data in A are the same as the level walking data in Fig. 8A of Carlson-Kuhta et al. (1998). 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), 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 paw liftoff (|) and then averaged over 16-26 steps. EMG records with similar cycle periods were selected for each grade; average cycle periods were 711 ± 12 ms for level treadmill walking (0.5-0.6 m/s), 567 ± 30 ms for 25% grade, and 446 ± 9 ms for the 75% grade. ⋮, estimated times for paw contact. The FHL, EDL, and TA data are from cat 3 and the FDL, PLT, FDB, and EDB data were from cat 5. The data in A are the same as in Fig. 9A of Carlson-Kuhta et al. (1998). For each muscle, voltage calibration bars marked on the right side are the same for all 3 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.

MUSCLES WITH STANCE-RELATED ACTIVITY ONLY. Four hindlimb muscles, each with extensor functions at knee (VL) or ankle (LG, PLT, FHL) joints had stance-related activity only. During level walking, these muscles were active just before paw contact and their activity continued throughout most of stance. At increased grades of downslope walking, the amplitude of the stance-related activity decreased and the relative duration of their bursts declined from 50-60% of the step cycle at the two lower grades to 15-17% of the cycle at the two steeper grades (Figs. 8 and 9).

For level walking the RF was also active only during stance, with the RF burst beginning around midstance (Fig. 8A). The onset of the RF burst shifted to the very beginning of stance as illustrated in Fig. 8, B-C, for walking at the 50 and 100% grades. This shift was also typical of downslope walking at the 25% grade. The RF EMG increased markedly at the steeper slopes (Fig. 8) and persisted for most of stance.

MUSCLES WITH PRIMARILY SWING-RELATED ACTIVITY. Activity of the ST and FDL was typically associated with swing-related actions. The ST had two bursts of activity that centered around paw liftoff and paw contact. The paw-liftoff burst (STpo) increased in amplitude and duration, particularly at the two steeper grades (Fig. 8C). At the 25% grade the STpo burst occupied 17-20% of the cycle, and the same burst occupied 40-50% of the cycle at the 100% grade. The amplitude of the paw-contact burst (STpc) was markedly lower than the amplitude of the STpo burst. Occasionally, low-level ST activity persisted throughout stance, and there was no pause separating the stance-phase activity from the onset of the STpo burst (Fig. 8C).

The FDL typically had one brief (24 ± 10 ms, mean ± SD)burst of activity just before paw liftoff during level walking. This burst increased in amplitude and duration at the steeper slopes (57 ± 27 ms at the 75% grade) of downslope walking. FDL activity during stance, if it occurred, was typically a low-level, tonic activity that tended to increase in amplitude during the steeper grades of downslope walking (seeFig. 9C).

MUSCLES WITH STANCE- AND SWING-RELATED ACTIVITY. Five muscles (EDB, FDB, EDL, TA, and IP) had both stance- and swing-related activity during downslope walking. The EDB, usually inactive during the stance phase of level walking, showed a progressive increase in stance as the grade increased (Fig. 9). The FDB, conversely, had bouts of activity during swing and stance-related activity during level and downslope walking. FDB activity progressively increased in amplitude with steeper inclines of downslope walking, particularly during stance (Fig. 9).

The swing-related activity of the EDL and TA was similar at all grades of downslope walking; however, stance-related activity (absent during level walking) was minimal at the lowest grade and substantial at the steepest grade (Fig. 9). During stance, both muscles were recruited around the time that the activity of the ankle extensor muscles (FHL, PLT) ceased. At the steeper slopes, EDL activity began soon after paw contact (~25-30 ms) and was followed by TA activity (~65-75 ms after contact). The activity of both muscles was substantial at midstance but declined markedly before the onset of their typical swing-related bursts (Fig. 9C).

The primary flexor of the hip joint, the IP, had only swing-related activity during level walking but exhibited a second burst of activity during the stance phase of downslope walking (Figs. 8 and 9). The swing-related burst of the IP was similar in amplitude and duration, lasting 30% of the step cycle for level walking at all grades of downslope walking. Conversely, the stance-related IP burst increased in amplitude at the steeper grades, but the burst duration at ~55% of the cycle was the same at all grades (Fig. 8, B and C). At the steepest slope, the IP burst amplitude during stance was markedly greater than the amplitude of the IP burst during swing (Fig. 8C).

MUSCLES WITH NO ACTIVITY. Although the two hip extensor muscles (ABF and ASM) were active during the stance phase of level walking, neither muscle was active during downslope walking at grades of 25-100% (Fig. 8). These results were unexpected and prompted us to study downslope walking at lower grades on the treadmill to ascertain if these muscles were inactive during downslope walking at any grade or if the lack of activity was associated with grades of 25% and higher.

Downslope treadmill walking: grades 5-25%

Two cats were tested on the treadmill at five grades (5-25%). For all grades, the average cycle periods were similar and ranged from 608 to 713 ms, with 65 ± 3% of the cycle period devoted to stance. EMG records are shown in Figs. 10 and 11.


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FIG. 10. Rectified-average EMG records for level (A, 0%) and downslope walking on the treadmill (0.6 m/s) at 2 grades of downslope walking (B, 10%; C, 20%). Windows of EMG from 10 steps were averaged by triggering from the time of paw liftoff (|); data are from cat 7. For each muscle, voltage calibrations are the same for all records: VL and ASM (0.2 mV), IP (0.4 mV), and ABF (0.6 mV). Horizontal timescale, 50-ms intervals.


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FIG. 11. Example of hindlimb kinematics and EMG for downslope walking at a 5% grade on the treadmill (0.6 m/s). Two steps are taken from cat 6; the record begins with PO of the 1st step and ends with PO of the 2nd step. |, each paw liftoff; ⋮, each paw contact; sount-west-arrow , marked reduction of hip extensor activity during the 2nd step; see text for details. Calibrations: horizontal, 100 ms; vertical, 0.2 mV.

At the 10% grade the ABF (Fig. 10B) and ASM activity were typically absent, but both of these muscles had "facultative" activity at the 5% grade. Facultative activity, different from step to step, is illustrated in Fig. 11. Here, both the ABF and ASM were active for the first step but inactive during most of the second step, except for a brief spike of activity soon after paw contact (Fig. 11, sount-west-arrow ). In this trial for cat 7, the ABF and ASM muscles were active in some steps but not in others with no apparent relationship to the hip-joint kinematics.

The IP of cat 6 did not have a consistent stance-related burst until the 15% grade. At the 10% grade there was often a brief bout of IP activity after the onset of stance (Fig. 10B). At the 20% grade, IP activity usually occurred within 50-70 ms after paw contact (Fig. 10C). The IP for cat 7 also lacked a consistent stance-related burst until the 15% grade, but at the two lower grades (5 and 10%) and occasionally during level treadmill walking, the IP exhibited a low level of tonic activity during most of stance (Fig. 11).

At the 10% grade the RF burst was similar in timing and shape to that recorded at the lowest slope (5%) and level walking (Fig. 10) The shift in the onset of the RF burst from midstance to earlier in stance occurred progressively from the 15% to the 25% grade. At the 20 and 25% grades, peak RF activity still occurred after midstance. The activity of the VL, in contrast, showed little change in amplitude or timing with treadmill walking at grades of 0-25%.

The kinematic data illustrated in Fig. 11 was typical of cat 6 at downslope grades from 5 to 25% on the treadmill. During stance the knee joint continued to flex (yield) and there was only a brief period of E3 extension. This kinematic pattern was also typical for some cats during overground downslope walking, as illustrated in Fig. 5B for the 50 and 100% grades.

    DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References

Slope-related changes in posture, gait, and hindlimb dynamics

During downslope walking the body mass must be moved downward and forward, both aided by gravity, without slipping on the inclined walkway. We covered the walkway surface with a thin, nonskid mat (see METHODS) (see also Carlson-Kuhta et al. 1998) to eliminate paw slippage at the steepest grade that occurred in one of two cats tested in a pilot study. With the nonskid mat the paws did not slide. Nonetheless, each cat adjusted its posture and limb orientation in ways that would increase the braking forces at the steeper grades. Although we did not assess stance-phase kinetics, our data provide some useful predictions.

Changes in the hindlimb kinematics at the steeper grades of downslope walking were consistent with the reduction of propulsion during stance. The duty cycle (e.g., the percent of cycle devoted to stance) decreased at the steepest grades and the range of stance-phase extension decreased at three joints (knee, ankle, and MTP). Also, the entire hindlimb stride shifted anteriorly with respect to the hip joint at the 50% grade and higher. This is an important adjustment because propulsive forces are associated with the portion of stance in which the hindpaw is posterior to the hip joint for forward walking (Fowler et al. 1993). For upslope walking the hindlimb stride shifted in the opposite direction, and there was a greater range of stance-phase extension at all four hindlimb joints (Carlson-Kuhta et al. 1998); thus the percent of stance devoted to propulsion most likely increased.

We anticipated that the anterior placement of the hindpaw would increase appreciably at the steeper grades of downslope walking, but it did not. This expectation was based, in part, on the assumption that a greater anterior placement would be associated with a larger braking impulse at the beginning of stance. Although there were modest increases in the anterior placement of the hindpaw at contact, the increases were not slope related (Fig. 4, Da). The cats' gait selections appeared to be one reason why the increases were not slope related. Cats typically used a lateral sequence to walk downslope. With this gait the ipsilateral hindpaw was placed very near the spot on the walkway that the ipsilateral forepaw was placed, as shown in Fig. 1A. If the hindpaw's anterior placement increased too much, the ipsilateral paws might actually collide. Such a collision could be prevented if the cat crouched to extend the forepaws anteriorly or if the cat shifted to a pacelike walk. Both tended to occur during downslope walking at the steeper slopes, as shown in Fig. 1C.

Others report that cats rarely if ever use pace walking for overground locomotion in their natural habitats (Blaszczyk and Loeb 1993; Hildebrand 1976). These authors suggest that pacing is only used by cats during novel or demanding situations, because pacing is associated with a greater roll of the body from side to side and is less stable than other gaits. Our data suggest that downslope walking at the steeper grades may be one of those demanding situations. In our testing setup each cat took only five or six steps down the steep walkway, and given the short distance and the fact that each cat crouched to lower its center of mass to increase its overall stability, decreases in lateral stability associated with pace walking may not have been at issue.

Although the level of hindquarter crouch was similar for downslope, upslope (Carlson-Kuhta et al. 1998), and crouched walking (Trank et al. 1996), adjustments in the orientation of the hind- and forelimbs were different and well suited to each form of locomotion. For downslope walking at the steeper slopes, the hindpaw placement was extended rostrally, but during upslope and crouched walking there was a decrease in the anterior hindpaw placement. The forepaw placement during downslope walking was extended rostrally, whereas there was no apparent change in the forepaw placement during upslope and crouched walking. It is probable that each forelimb provided only a braking force for most, if not all, of the stance phase during downslope walking. This prediction is based in part on the observation that the orientation of the cats' forelimbs for downslope and backward level walking are similar. During the stance phase of backward walking, the forelimbs produce a continuous shear component ground-reaction force that would constitute a braking force during forward walking (see Fig. 5C of Perell et al. 1993). The function of the forelimbs during downslope walking deserves a comprehensive analysis.

Motor pattern changes associated with downslope walking

Based on the assumption that the requirement for propulsive forces would be less during the stance phase at the steeper slopes of downslope walking, we anticipated that extensor activity would decrease over the range of grades tested. Our EMG data, as well as force-buckle and EMG data reported by Herzog et al. (1993) for level and downslope (10° incline) walking, show that the recruitment of the MG and PLT, but not the soleus, were consistent with this prediction. We did not expect hip extensor muscles to be totally inactive at most grades of downslope walking, nor did we expect hip flexor muscles to be active during stance. Furthermore, we did not anticipate that the knee extensor EMG activity would be similar in amplitude at all grades. We focus here on these three unexpected findings, as well as the co-contraction of the digit muscles.

MOTOR PATTERNS OF HIP-JOINT MUSCLES DURING STANCE. The hip joint extended throughout stance of downslope walking, and the range of extension was similar at all grades tested; however, the primary, uniarticular extensor muscles of the hip joint (ABF and ASM) were inactive at all grades of overground downslope walking and at grades of treadmill downslope walking steeper than 15%. These results suggest that in contrast to level walking, extension at the hip joint may not be associated with an extensor muscle torque during the stance phase of downslope walking at grades >= 15%. For level walking an extensor torque at the hip joint is associated with the recruitment of hip extensor muscles during the first half of stance. At midstance, however, the hip-joint torque becomes flexor and the reversal is associated with the onset of RF activity and a period in which the resultant ground-reaction vector is oriented posterior to the hip joint (see Fig. 6A of Perell et al. 1993). As a consequence of these dynamics, power is generated at the hip joint for the first half of stance and then is absorbed during the second half of stance, as the rate of hip extension is slowed (see Fig. 9A of Perell et al. 1993).

During overground downslope walking, activity of the hip flexor muscles (IP and RF) always replaced the activity of the hip extensor muscles (ABF and ASM). Because the hip joint continued to extend in the face of hip flexor contraction, it is likely that power was absorbed throughout the stance phase as the muscles undergo a lengthening (eccentric) contraction. Similar conditions exist when the cat walks backward; the hip joint extends while hip flexor muscles are active, and power is absorbed at the hip joint for most of stance (see Fig. 9B of Perell et al. 1993).

Our EMG data for hip-joint muscles lead us to predict that there will be no extensor torque at the hip joint during the stance phase of downslope walking at grades >= 15%. Preliminary kinetic data from R. Gregor's laboratory (Smith et al. 1997) appear to support this prediction at three grades (25, 50, and 75%) of downslope walking. They found that a flexor muscle torque dominated the kinetic profile of the hip joint during the stance phase of downslope walking except for an extensor torque around paw contact that is brief in duration and usually small in magnitude. The finding of a flexor muscle torque is consistent with the lack of extensor muscle activity and the onset of flexor muscle activity at the hip joint during the early phase of stance.

MOTOR PATTERNS OF A KNEE-JOINT EXTENSOR DURING STANCE. The VL was active during stance of downslope walking at all grades tested on the treadmill and the walkway, and there was little change in the amplitude or duration of the VL burst. The VL EMG data and the absence of knee flexor muscle activity during the stance phase of downslope walking suggest that the extensor muscle torque at the knee joint might have a similar profile over a wide range of downslope grades. Preliminary data from R. Gregor's laboratory (Smith et al. 1997) showed an extensor torque at the knee joint during the stance phase that was similar in magnitude and duration for three grades (25, 50, and 75%) of downslope walking. In contrast, they found that the peak muscle torque at the knee joint associated with upslope walking increased substantially for the same three grades (R. Gregor, unpublished data). These findings for upslope walking are consistent with a marked increase in VL EMG at the steeper grades of upslope walking (Carlson-Kuhta et al. 1998).

STANCE MOTOR PATTERNS OF DISTAL MUSCLES. The duration of extensor muscle activity at the ankle joint (LG, PLT, and FHL) decreased markedly at the steeper grades. These data suggest that the duration of the extensor muscle torque, which predominates the kinetic profile of the ankle joint during level walking (Fowler et al. 1993; Perell et al. 1993), occupies less of the stance phase of downslope walking, particularly at the steeper grades. The ankle flexor muscles (TA and EDL) remained reciprocally active with the ankle extensor muscles, and there was a tendency for EDL to be recruited around midstance at the steeper slopes.

At the 25% grade the recruitment patterns of the two intrinsic muscles of the paw, the EDB and FDB, were similar to that for forward, level walking. Typically, the EDB is active only at the end of swing for level walking (see Trank and Smith 1996), but for upslope walking at the 75% grade (Carlson-Kuhta et al. 1998), backward walking on a level treadmill (Trank and Smith 1996), and downslope walking at the 75% grade, the EDB is recruited for most of stance. The purpose of the FDB-EDB co-contraction during stance for these forms of walking is not clear and warrants further study.

Neural control of slope walking by a multifunctional CPG

In 1981 Grillner proposed a model for a spinal central pattern generator (CPG) that included separate control units for flexor and extensor muscles at each hindlimb joint. He hypothesized that each unit contained all the neural elements required (except for tonic facilitation by descending supraspinal fibers) to generate locomotor-like bursts without sensory feedback or patterned input from supraspinal centers. One advantage of Grillner's model is that the array of units can be connected in different ways to program various walking forms or even different cyclic motions such as walking and scratching (also see Gelfand et al. 1988). We illustrate in Fig. 12 how Grillner's unit-burst generator model can be used to account for changes in the organization of muscle synergies that distinguish downslope and upslope walking from level walking.


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FIG. 12. Three central pattern generator (CPG) configurations for the control of cat hindlimb muscles during level and slope walking. The CPGs are patterned after the model proposed by Grillner (1981). Each large circle represents one unit-burst generator (called a unit) for the control of extensor (EX) or flexor (FX) muscles of the hip, knee, ankle, or foot joints. Striped circles represent units that act together during stance, whereas half-striped circles represent dual-phase units that generate stance-related and swing-related activity. In B, X represents lack of hip extensor activity during downslope walking, thus the inactivity of the hip extensor unit. Excitatory connections between units are represented by small open circles, whereas inhibitory connections are shown by small shaded circles. Hamstring muscles are placed in the knee flexor unit (indicated by ST). Muscles of the foot are placed according to their physiological functions described Engberg (1964); the FDB is a physiological extensor and the EDB is a physiological flexor. The placement of the EDL, FHL, and FDL, as well as other muscles hindlimb, are presented in the DISCUSSION.

CPG UNITS FOR THE CONTROL OF HIP- AND KNEE-JOINT MUSCLES. The excitatory coupling between the hip and knee extensor units, illustrated in Fig. 12A, creates a robust extensor synergy that is typical of forward and backward walking (in contrast to Grillner's 1981 prediction) (see Buford and Smith 1990), upslope walking (Fig. 12C), and crouched walking (Trank et al. 1996). During downslope walking, however, the extensor synergy is disrupted as the hip extensor muscles are not recruited at grades >20%. To model the lack of hip extensor activity at these grades, we have replaced the excitatory connections between the hip and knee extensor units with an inhibitory connection (Fig. 12B). With this altered connection and the inhibition provided by the hip flexor unit, the hip extensor unit will be inactive for most, if not all, of the step cycle (Fig. 12B, X).

During downslope walking the IP exhibited two bursts, one during stance (the "unexpected" burst) and one during swing (the "usual" burst). Most muscles have only one burst during a single-step cycle, except the ST and its synergist that have one burst at the end of stance and one at the end of swing. Grillner (1981) modeled the two ST bursts by inhibiting the ST unit with inputs from the adjacent units (Fig. 12A); thus the ST unit was released from inhibition during a brief period at the end of stance and another at the end of swing. We could not use the same solution to model the two IP bursts because one burst coincided with the main period of extensor activity and the other with the main period of flexor activity. To model this we have added a diagonal excitatory connection between the knee extensor and the hip flexor units while maintaining the excitatory connections between the ankle and hip flexor units (Fig. 12B). By doing this we have created a "dual-phase" unit, one that generates both extensor- and flexor-related activity. This type of unit was not featured in Grillner's 1981 model.

The coactivity between the IP and the VL during downslope walking is a rare example of a "mixed synergy" that is similar to the coactivity of the VL and the TA during paw shaking (Smith et al. 1985). The mixed synergy for the locomotor CPG is modeled by a diagonal excitatory connection (Fig. 12B), and this design is similar to the diagonal excitatory connection between the knee extensor and ankle flexor units proposed by Carter and Smith (1986; see their Fig. 7B) for the paw-shake CPG. Pearson and Rossignol (1991) demonstrated that neither feedback nor input from supraspinal centers was necessary for the mixed synergy of paw shaking to be elicited. They elicited the VL-TA coactivity in a spinalized, immobilized preparation by squirting the hindpaw with water. With regard to fictive locomotion, the IP muscle has not been studied to any extent, and we do not know if the IP-VL coactivity can be generated centrally.

Although the hip units are the focus of change for the control of downslope walking, the knee units are the focus of change for the control of upslope walking. Our EMG data for upslope and downslope walking at the steep grades (75 and 100%) suggest that STpo activity was prolonged and similar to the swing-phase activity of the TA. We have modeled this by changing the connection between the ST unit and the ankle flexor unit from inhibitory to excitatory (Fig. 12, B and C). Also, ST activity often occurred during the stance phase at the steep slopes of upslope walking, and we have modeled this additional bout of activity by replacing the inhibitory connection between the knee extensor and ST units with an excitatory connection (Fig. 12C). With this change we have created another dual-phase unit that generates separate bursts of activity during swing and stance. Given that the ST unit is excited by all adjacent units in this CPG model, it is possible that ST activity will continue through most of the cycle during upslope walking. Some of our ST records at the 100% grade actually show continuous activity during most of the cycle, except for a brief interval after midswing when the hip and knee flexor activity is waning and knee extensor activity is waxing (see Fig. 10C of Carlson-Kuhta et al. 1998).

Does ST activity occur with extensor-related activity during fictive locomotion? When fictive locomotion is elicited with dopamine in acutely spinalized, immobilized cats, ST activity coincides with TA activity (Grillner and Zangger 1979; Pearson and Rossignol 1991), but spontaneous locomotor-like motor patterns in the decorticated, immobilized cats are characterized by ST bursts that alternate with flexor bursts (Perret and Cabelquen 1976, 1980). That ST fictive motor patterns are preparation specific suggests that spinal networks may be reconfigured, as proposed in Fig. 12, by supraspinal input in the absence of feedback.

CPG UNITS FOR THE CONTROL OF ANKLE-JOINT AND DIGIT (FOOT) MUSCLES. The extensor muscles (LG, PLT, and FHL) of the ankle joint participate in the extensor synergy with the hip and knee extensors during forward walking, and they are reciprocally active with the flexor muscles (TA and EDL) of the ankle joint. These patterns of activity are unchanged for upslope walking; thus the circuits in Fig. 12, A and C, are similar. It is important to note that we have placed the control of the FHL and the EDL muscles in the CPG units that are consistent with their actions at the ankle joint (which are opposite to their actions at the digits). These placements are consistent with our EMG data and with Engberg's (1964) classification of the FHL as a "physiological extensor" and the EDL as a "physiological flexor."

For downslope walking we have changed the ankle unit connections to reflect our EMG data. The ankle extensor muscles, unlike the knee extensors, exhibit only a brief burst that is centered around paw contact, and ankle flexor activity is initiated soon after midstance. We have attempted to show the change by making an inhibitory connection between the knee and ankle extensor units while maintaining the inhibitory connection between the ankle flexor and extensor units (Fig. 12B). By doing this we have inhibited the ankle extensor unit for most of the cycle, releasing it when flexor activity is waning and extensor activity waxing.

Grillner's (1981) model included a flexor unit and an extensor unit for the foot muscles as well as a separate, unpaired unit for the EDB (aligned with the extensor units). In Fig. 12A we have placed the control of the EDB in the foot flexor unit and the FDB in the foot extensor unit. Our placement of muscles reflects their EMG activity patterns and their physiological functions during various foot reflexes (Engberg 1964).

The principal burst of the FDB occurs during stance for level and slope walking, and this activity is part of the overall extensor synergy. We have modeled this by excitatory connections between the foot extensor and the ankle extensor units for level and upslope walking (Fig. 12, A and C). To facilitate a longer FDB burst for downslope walking, we have created an excitatory connection between the foot extensor and the knee extensor units. The FDB also has swing-related activity; to model this we have added an excitatory diagonal connection between the foot extensor unit and the ankle flexor unit (Fig. 12). For all three models in Fig. 12 we created a dual-phase unit for the FDB, one that generates extensor- and flexor-related activity.

Although the anatomy of the FDL muscle is similar to that of the FHL muscle (O'Donovan et al. 1982), the FDL's activity patterns are similar to those of the FDB (Trank and Smith 1996). For this reason, we propose that the FDB and FDL may be controlled by the same unit in the locomotor CPG. Although the FDL has a flexor and an extensor burst during level walking, the FDL extensor-related activity is more of a facultative feature of its pattern during level walking (see O'Donovan et al. 1982; Trank and Smith 1996). Being facultative, it is likely that the FDL extensor-related burst is facilitated by external conditions triggered by sensory feedback, such as cutaneous stimulation (see Moschovakis et al. 1991). However, FDL activity also occurs during flexor- and extensor-related phases of fictive locomotion (Fleshman et al. 1984), suggesting that the FDL unit, similar to that proposed for the FDB unit in Fig. 12, is facilitated by central mechanisms that generate dual-phase patterns of activity.

During level walking the EDB is active during the last half of swing, whereas the FDB is active during the first half of swing. We have modeled this with a reciprocal inhibitory connection between the EDB unit and the FDB unit (Fig. 12A). During downslope and upslope walking, the EDB is also active during stance, and we have represented this by replacing the inhibitory connection with an excitatory connection from the FDB unit to the EDB unit (Fig. 12, B and C). In doing so, we have created a dual-phase unit for the EDB that generates both flexor- and extensor-related activity during the locomotor cycle.

During fictive locomotion EDB activity is usually coincident with the activity of flexor muscles in acute spinalized and decerebrate cats (Grillner and Zangger 1975, 1984). But during spontaneous locomotion in the decorticated cat, EDB activity was coincident with extensor-related activity, and this activity persists after curarization with gallamine triethiodide (Flaxedil) and hindlimb deafferentation (Perret and Cabelquen 1980). Taken together these results suggest that the CPG unit for the EDB may generate activity during the flexion or extension phase; this is consistent with our findings for slope walking and our CPG model in Fig. 12.

MULTIFUNCTIONAL CPG AND FUZZY CONTROLLERS. Although the unit-burst model may account for the reorganization of muscle synergies, it does not account for the precise timing or the relative output of activity to each muscle within a synergy. It is probable that the CPG output to motoneuron pools is reinforced by sensorimotor responses at the spinal level that can be gated by higher centers for specific tasks. For example, discharges of group I afferents from ankle extensors facilitate the recruitment of extensor muscles at the hip, knee, and ankle during locomotion induced by stimulation of the mesencephalic locomotor region, but the same discharges inhibit extensor recruitment when the cat is at rest (Guertin et al. 1995; McCrea et al. 1995; Whelan et al. 1995). A brief tap to the paw dorsum at the beginning of swing elicits a stumbling corrective response during forward but not backward walking (Buford and Smith 1993). For backward walking, a stumbling response is elicited when the plantar surface of the paw is tapped at the onset of swing. In both cases the tap mimics an obstruction to the paw's swinging motion, and the initial response withdraws the hindpaw from the unexpected object by ankle extension or flexion.

Prochazka (1996) suggested that the nervous system may act like a "fuzzy controller" to combine multiple sensory inputs according to rules for the production of the appropriate sensorimotor responses. This analogy is particularly apt for discussing the control of hindlimb locomotion. The rules for effecting the transition from stance to swing, for example, might be different for different forms of walking. During level walking, hip flexion is initiated if the hip is extended and the ankle extensors are not contracting and the contralateral limb is loaded (bearing weight). The same if-and rule may apply to backward and upslope walking, but the weighting or combination of sensory inputs may be evaluated differently. The hip joint will be less extended when the ankle extensors stop contracting during backward walking (Buford and Smith 1990) and more extended when the ankle extensors stop contracting during upslope walking (Carlson-Kuhta et al. 1998). For downslope walking the ankle extensors may not be active after paw contact, but the hip continues to extend.

If rule-based control of walking occurs, we need to understand how the rules are set; supraspinal input at the spinal level would likely be important. For example, the animal's behavioral goal (e.g., walking downslope or upslope), governed by supraspinal centers, may be responsible for issuing a set of rules for different forms of walking much in the same way that descending inputs to the stomatogastric ganglion set the network's configuration and the effects of sensory inputs (see Harris-Warrick et al. 1997). By setting rules that reconfigure the CPG (see Fig. 12) and facilitate key interneurons for task-specific sensorimotor responses (see Fig. 8 of McCrea et al. 1995; Fig. 8 of Pearson and Collins 1993), inputs from higher centers would be able to control different forms of locomotion at the segmental level without providing an extensive set of motor instructions for each.

    ACKNOWLEDGEMENTS

  We thank S. Lauretz (Animal Health Technician) for assistance with surgery, animal care and training, and data collection; C. Chen for assisting with the gait analyses and working on many of the figures; S. Fornalski and P. Lim for assisting in the data collection and analysis of the treadmill downslope data; and K. Veling for assisting in the data collection and the preliminary analyses of the walkway slope data. 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 related to limb dynamics.

  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.

    FOOTNOTES

  Address reprint requests to J. L. Smith.

  

    REFERENCES
Abstract
Introduction
Methods
Results
Discussion
References

0022-3077/98 $5.00 Copyright ©1998 The American Physiological Society