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Reactive and anticipatory control of posture and bipedal locomotion in a nonhuman primate
Progress in Brain Research, Vol. 143 ISSN 0079-6123 Copyright ß 2004 Elsevier BV. All rights reserved
CHAPTER 19
Reactive and anticipatory control of posture and bipedal locomotion in a nonhuman primate Futoshi Mori1,*, Katsumi Nakajima1, Atsumichi Tachibana1, Chijiko Takasu1, Masahiro Mori1, Toru Tsujimoto2, Hideo Tsukada3 and Shigemi Mori1 1
Department of Biological Control System and 2Center for Brain Experiment, National Institute for Physiological Sciences, Okazaki 444-8585, Japan 3 PET Center, Central Research Laboratory, Hamamatsu Photonics KK, Hamakita 434-8601, Japan
Abstract: Bipedal locomotion is a common daily activity. Despite its apparent simplicity, it is a complex set of movements that requires the integrated neural control of multiple body segments. We have recently shown that the juvenile Japanese monkey, M. fuscata, can be operant-trained to walk bipedally on moving treadmill. It can control the body axis and lower limb movements when confronted by a change in treadmill speed. M. fuscata can also walk bipedally on a slanted treadmill. Furthermore, it can learn to clear an obstacle attached to the treadmill’s belt. When failing to clear the obstacle, the monkey stumbles but quickly corrects its posture and the associated movements of multiple motor segments to again resume smooth bipedal walking. These results give indication that in learning to walk bipedally, M. fuscata transforms relevant visual, vestibular, proprioceptive, and exteroceptive sensory inputs into commands that engage both anticipatory and reactive motor mechanisms. Both mechanisms are essential for meeting external demands imposed upon posture and locomotion.
Introduction
commands; an execution center for the initiation, sustenance, goal-directed modification and termination of locomotion (Mori, 1997; S. Mori et al., Chapter 33 of this volume); and, a central program, which integrates selected cognitive and emotive information and stores it as ‘locomotor memory’ (McFadyen and Be´langer, 1997). These centers appear to reside within the cerebellum, basal ganglia and cerebral cortex, and their interconnecting pathways (Brooks and Thach, 1981; Armstrong, 1986; Garcia-Rill and Skinner, 1987; Kably and Drew, 1998; Mori et al., 1999b). By integration of these lower- and higher-control mechanisms, Bp and quadrupedal (Qp) animals continuously adjust their posture and locomotion, and respond appropriately to environmental perturbations.
The elaboration of bipedal (Bp) locomotion by the human and selected nonhuman primates requires that the central nervous system (CNS) recruit and integrate lower-order automatic and higher-order volitional control mechanisms. Lower-order control is comprised of several posture- and locomotorrelated subprograms stored in the brainstem and spinal cord (Mori, 1987; S. Mori et al., Chapter 33 of this volume). Conceptually, higher-order control involves at least three major subsystems: an integration center for postural and locomotor *Corresponding author: Tel.: þ 81-564-55-7772; Fax: þ 81-564-52-7913; E-mail: [email protected]
191 DOI: 10.1016/S0079-6123(03)43019-7
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Accommodation to the external environment requires both reactive and anticipatory control mechanisms, which are presumed to reside in lower and higher parts of the CNS, respectively (Wall et al., 1981; Mori, 1987; Patla et al., 1991; Lange et al., 1996; McFadyen and Be´langer, 1997). The use of these two CNS mechanisms provides the basis for successful Bp navigation on slanted, uneven and obstacle-impeded walking surfaces, all with a seamless integration of total posture and movement of individual motor segments. For this, the CNS must take into account the ongoing state of the spinal mechanisms and locomotor apparatus, e.g., the phase of the locomotor cycle (Arshavsky et al., 1986). In addition, CNS-controlled, visuomotor coordination is apparently one of the key factors for the successful execution of unaided locomotion (Georgopoulos and Grillner, 1986; Drew, 1991; Patla et al., 1991). Inadequate incorporation of proprioceptive, exteroceptive, visual and vestibular information into the motor commands from the integration center may be one of the causes of disintegration of a number of motor segments, thereby resulting in stumbling and other unstable forms of locomotion. We have recently shown that the Japanese monkey, Macaca fuscata, is a valuable nonhuman primate Bp model for potentially advancing understanding of CNS mechanisms that contribute to the control of postural and locomotor behavior (Mori et al., 1996; Nakajima et al., 2001). This animal is normally Qp but it can be operant-trained to use Bp locomotion on the surface of a moving treadmill belt. In the latter mode, we have recently examined M. fuscata’s reactive and anticipatory motor behavior during various walking tasks. It should be mentioned here that the monkey’s Bp walking is digitigrade and it differs from the plantigrade walking of humans, which is characterized by heel-strike and toe-off (Carlso¨o¨, 1972). Nevertheless, both single and double support phase by the lower limbs were observed during execution of monkey’s Bp walking. In the following sections, we first present a kinematic analysis of the animal’s reactive capability during Bp locomotion on a slanted treadmill belt (Mori et al., 1999a). Next, we show its anticipatory and reactive capability when accommodating an obstacle on a horizontal treadmill belt (Mori et al., 2001a; see also Nakajima et al., Chapter 18 of this volume).
Reactive locomotor patterns during slanted walking Bp locomotion in humans and nonhuman primates must simultaneously meet several requirements, including: (1) antigravity support, (2) stepping movements, (3) equilibrium and (4) propulsion (Martin, 1967; Mori, 1997). The force for the latter is provided by the weight of the body ‘sliding down an incline’ with forward movement. To accommodate a constantly changing environment, the neural mechanisms for the requirements must be coordinated. For example, uphill and downhill (slanted) Bp walking by humans require specific modifications in lower-limb kinematics and the supporting body posture (Martin, 1967; Brandell, 1977; Wall et al., 1981; Kawamura et al., 1991; Lange et al., 1996; Leroux et al., 1999). In uphill versus level walking, the legs need to generate a larger acceleration force in order to transfer the center of body mass forward. In parallel, postural adjustments are also required to maintain body equilibrium and facilitate generation of forward propulsive force. In downhill walking, the legs need to generate a net deceleration force to brake forward transfer of the center of body mass. Again, postural adjustments facilitate this braking. We have examined these responses during the skilled Bp locomotion of M. fuscata with a focus on the extent to which its movements resemble those of the human. Prior to slanted walking, M. fuscata was operanttrained to use both a Qp and Bp gait while walking on a level treadmill belt at different speeds (for methods, see Mori et al., 1996; Nakajima et al., 2001). Once mastered, the animal was challenged with slanted tasks. Figure 1 shows the exemplary walking patterns of M. fuscata on uphill ( þ 15 ) and downhill (15 ) grades at a fixed treadmill speed (1.3 m/s). Superimposed on the drawings are exemplary walking patterns of the same monkey on a level grade at the same treadmill speed. Lines have been drawn on the animal sketches to depict relevant kinematic and joint angles: ear–hip angle and the angles at the hip, knee, ankle and metatarsophalangeal (MTP) joints. The line between ear and hip represents the body’s axis. Figure 1A–B show the instantaneous postural shift when the monkey placed the foot of its left,
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Fig. 1. Schematic drawings of M. fuscata during Bp level versus slanted walking at the same speed. Open drawings show body position and stride on a level (0 ) treadmill belt. Filled drawings show the same animal during uphill (A, þ 15 ) and downhill (B, 15 ) walking. In all cases, the belt speed was 1.3 m/s. In this and Fig. 2, the treadmill belt was moving from left to right, and the monkey was walking from right to left. Drawings are superimposed with reference to the hip joint. Arrows indicate the changes in body axis from level to uphill (A), and level to downhill (B) walking.
forward limb on the moving treadmill belt (i.e., touchdown; onset of the stance phase of the left limb). Next, the monkey lifted the foot of its right, rearward limb up from the surface of the treadmill belt (i.e., takeoff; onset of the swing phase of the right limb). In uphill walking (Fig. 1A), the monkey inclined its body axis maximally during the stance phase of both limbs. The extent of forward body axis inclination was much larger than that observed during level walking. Throughout a single uphill versus level step cycle, the monkey exhibited: (1) a larger flexion of the hip joint, lesser extension of the knee joint and a larger ankle dorsiflexion during the mid-swing and early stance phase; and (2) a larger knee joint extension in the late stance phase. In downhill walking (Fig. 1B), the monkey declined its body axis maximally during the stance phase of both limbs. The extent of body axis declination was much larger than that observed during level walking.
Throughout a single downhill versus level step cycle, the monkey exhibited: (1) a larger extension of the knee joint and lesser flexion of the hip joint during the late swing and early stance phase; and (2) a lesser extension of the hip joint and larger flexion of the knee joint during the late stance and early swing phase. These coordinated hip–knee flexion–extension patterns were also observed in knee–ankle joints. Figure 1 also shows that forward inclination and backward declination of the body axis increased proportionately with an increase in treadmill angle (upward or downward, respectively) and treadmill speed. An uphill increase in treadmill angle from 0 to 7 to 15 at a constant treadmill speed resulted in an increase in the maximum degree of forward inclination from 15 to 24 to 37 at a fixed treadmill speed (1.3 m/s), respectively. Similarly, a downhill increase in treadmill angle from 0 to 7 to 15 at the same treadmill speed resulted in a decrease in the maximum
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inclination degree of body axis from 15 to 8 to 2 , respectively. This relationship between changes in treadmill angle and maximum inclination/declination of the body axis was near linear across all three of the tested treadmill speeds (0.7, 1.0 and 1.3 m/s). During level treadmill walking at a fixed speed (0.7 m/s), the duration of the stance and swing phase of the step was 0.60 and 0.25 s, respectively. Uphill and downhill walking involved more prolonged and shortened stance-phase duration, respectively. This relationship was maintained across the tested treadmill speeds. The duration of the swing phase of the step did not change significantly, however. We found a linear relationship between treadmill angle and stride length, i.e., a progressively longer stride for an increase in treadmill angle from 15 to þ 15 . We also found associations between stride length, treadmill angle and treadmill speed. During uphill walking, step-cycle frequency decreased as stride length and treadmill speed was increased, the reverse occurring during downhill walking. Healthy humans make quite similar adjustments to those described for slanted walking (Wall et al., 1981; Kawamura et al., 1991; Leroux et al., 1999). Taken together, these results suggest that the operant-trained Bp locomotion of M. fuscata is smooth and versatile under varying external conditions, and its functional coupling between the lower limbs and body posture is quite similar to that of humans. The results demonstrate that for Bp walking, the monkey has acquired optimal CNS parameters for the coordination of multiple motor segments during slanted walking.
Anticipatory and reactive adjustments during obstacle-encountered treadmill walking During everyday human locomotion, the feet often collide with unexpected obstacles, thereby requiring compensatory postural and gait adjustments to prevent stumbling and falling, and reestablish smooth walking. Such adjustments have been studied experimentally in the human by having the subject walk on an obstacle-obstructed pathway (Eng et al., 1994) or a moving treadmill belt (Schillings et al., 1996). Similarly, Dietz et al. (1987) studied stumbling-corrective reactions in humans by accelerating
and decelerating the speed of a treadmill belt. These studies all demonstrated that humans use both reactive and anticipatory postural adjustments to perturbations encountered while walking (McFadyen and Be´langer, 1997). Such adjustments occur in a proactive way during all phases of the step cycle, with visuomotor coordination a critical factor for anticipatory adjustments. In order to successfully judge distances and modify step length to attain a target or avoid an obstacle, the human needs but intermittent visual sampling of the immediate environment (Georgopoulos and Grillner, 1986; Drew, 1991; Patla et al., 1991). We have tested the extent to which M. fuscata can perform similarly during its Bp locomotion. Figure 2 shows that we trained M. fuscata to step over an adjustable-height rectangular block (width: 25 cm; length: 5 cm; height: 2.4, 5.0 and 7.0 cm) that was placed on the left side of a treadmill belt. The obstacle was arranged to confront the left limb every 4–6 steps, as dependent on belt speed. In this situation, the monkey could be motivated to walk continuously for 3–5 min, with such continuity termed a single trial. In a single trial, the monkey encountered the obstacle 40–70 times. A 3–4-min rest was needed between trials to insure that the animal maintained a relatively constant level of reward-based motivation (Mori et al., 2001a). Successive trials involved use of different combinations of fixed treadmill speed (0.7–1.3 m/s) and obstacle height. During initial trials, the monkey often stumbled when the toe of the trailing left foot stepped on the obstacle’s top (horizontal) surface, or slipped up on the initially encountered (vertical) surface. After several sequential trials, the number of stumbles in a single trial was reduced, i.e., the monkey gradually learned to clear the obstacle at various walking speeds, by use of what in humans has been termed a ‘hip–knee flexion strategy’ (McFadyen and Winter, 1991). This involved the monkey increasing the extent of flexion of the trailing left limb’s hip and knee joint while simultaneously, the leading right limb alone supported the center of body mass and maintained equilibrium. When the obstacle’s height was raised, there was a corresponding increase in hip/knee joint flexion of the trailing limb so as to produce sufficient clearance space above the obstacle.
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Figure 2A shows M. fuscata’s exemplary walking pattern during the control (no-obstacle) condition. Figures 2B–D show patterns observed at different times during the perturbation (obstacle-on) condition: B, with the in-coming obstacle 3–4 steps ahead and out-of-sight; and C, a successful clearance; and D, recovery after an unsuccessful clearance. In the control (Fig. 2A) state, the center of body mass was supported by the leading (right) limb alone when the trailing left limb was at its mid-swing phase with moderate flexion at the hip and knee joints. When the in-coming obstacle was still out-of-sight (Fig. 2B), but probably anticipated, the hip and knee flexion extent of trailing limb was more pronounced. This effect was exaggerated even further during successful clearance of the obstacle (Fig. 2C), which also included a further dorsiflexion of the ankle. When the animal encountered the obstacle during the period of early- to mid-swing phase, it easily cleared the obstacle. With some presumably visual information, it could adjust the trajectory of left foot even during the late period of swing phase and successfully clear the obstacle. Figure 2 does not
show that in this latter case, the trailing limb at the swing phase undertook a longer and more prolonged stride to maintain equilibrium. During this task, there was no significant change in the body’s axis, and the head was maintained at a relatively constant position. When the trailing foot failed to clear the obstacle (Fig. 2D), stumbling occurred routinely. Such stumbling usually involved either stepping on, or slipping up, the obstacle during the late swing phase of the trailing left limb’s step. Figure 2D shows the pronounced postural perturbation associated with slipping up the obstacle. Immediately after foot– obstacle contact, the monkey slightly moved its body axis backward. This was followed immediately by a rapid and pronounced ( 40 ) forward movement of the body axis. Subsequently, the animal: (1) shortened the swing period of the leading limb; (2) flexed the left and right lower limb joints to lower the center of body mass to the treadmill belt; (3) extended its left (and/or right) forelimb forward and/or downward; and finally (4) extended its lower limb joints to raise the lowered
Fig. 2. Schematic drawings of the mid-swing phase of the left hindlimb during normal versus obstacle-encountered, level Bp walking. (A) Control (no-obstacle) walking at 1.0 m/s. (B–D) Walking at the same speed, but in the obstacle-encountered situation. (B) Obstacle 3–4 steps ahead of monkey and out-of-sight. (C) A successful clearance of the obstacle; and (D) the defensive posture that occurred after stumbling over the obstacle.
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body mass to the preperturbed position. The first three compensatory reactions of multiple motor segments served to stabilize the perturbed posture. When the animal stepped on the obstacle, it immediately initiated a new trailing limb’s swing phase from the top surface of the obstacle. In such instance, landing of the leading right foot on the treadmill belt always preceded the beginning of the trailing limb’s swing phase. Alternatively, if the trailing limb’s foot slipped up the obstacle, the animal initiated the new swing phase from the belt surface. To clear the obstacle, the monkey adjusted the trajectory of the trailing limb with the toes fully flexed. These reactive compensations for the perturbed posture finally made the animal possible to restore the position of the head, body and limb segments to preperturbed one, and to walk safely and smoothly. Recovery of walking required the restoration of (1) the center of body mass, (2) the head position and (3) the body axis to its predisturbed position in space. Interestingly, the correction of the head position always occurred first, followed by that of the body axis and upper and lower limbs. Perhaps head position in space is a critical determinant of the nature and extent of reactive responses to postural perturbations encountered during walking. From the preceding paragraphs, it can be seen that M. fuscata recruited both anticipatory and reactive control mechanisms to prepare for the incoming obstacle, even when it was still out-of-sight, and to restore the perturbed posture after stumbling over the obstacle. The latter mechanism was also used to adjust the trajectory of the trailing limb with the integration of visual information and motor output. We have also observed that the occurrence of stumbling in a single trial decreased as the monkey encountered successive obstacles. Such observations suggest that the monkey could store a novel ‘obstacle clearance strategy’ in its ‘locomotor memory’ repertoire. This was presumably acquired by motor learning.
Comment and summary Overall, the kinematic analyses of M. fuscata’s Bp locomotion indicate that this animal and the human
have similar kinematics for the integration of posture and locomotion, particularly for the hip joint. In both, hip extension proceeds from touchdown (beginning of stance phase) to takeoff (beginning of swing phase) of the foot. When the Bp-walking monkey encountered an obstacle, it changed its foot trajectory to produce a larger-than-usual successful clearance over the obstacle (hip and knee flexion strategy). Moreover when the monkey stumbled over the obstacle, it quickly recovered from its perturbed posture and movement, and continued its smooth, well-coordinated Bp walking. These findings suggest that the monkey’s CNS received and transformed salient visual, vestibular, proprioceptive and exteroceptive sensory information into output (command) motor signals appropriate for the integration of multiple body segments, this being essential for successful accommodation of the obstacle. Such a transformation process, including recall of ‘locomotor memory’, would require continual modification of the ongoing postural and locomotor control signals, which include anticipatory and reactive components. The studies described earlier show that the normally Qp M. fuscata is a valuable nonhuman primate model for studying the CNS control of not only Bp locomotion and accompanying posture, but also compensations to stumbling and falling, and eventually several other types of movement disturbance. Shibasaki’s Kyoto University group has recently used single photon emission computed tomography (SPECT) to study corridor (Fukuyama et al., 1997) and treadmill (Hanakawa et al., 1999) walking by normal adult subjects. Their results have shown a high bilateral activation in the primary sensorimotor, supplementary motor- and visual cortex, as well as in the basal ganglia and cerebellum (see also Shibasaki et al., Chapter 20 of this volume). Presumably, the CNS of the Bp-walking monkey display analogous activation patterns. To test this idea, we have recently developed a noninvasive neuroimaging protocol. Positron emission tomography (PET; Watanabe et al., 1997) is being used to measure cerebral glucose metabolism after epochs of Bp locomotion. A preliminary study has already shown that multiple brain regions are activated (Mori et al., 2001b), just as they are in humans. Some of these brain regions may reflect plastic changes in neural circuitry involved in long-term locomotor
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learning. This PET project should provide the opportunity to study experimentally how each of the activated brain regions contributes to the control of Bp posture and locomotion, including reactive and anticipatory control mechanisms. It should also contribute to further understanding of CNS circuitry required for the initiation, maintenance and recall of Bp locomotion, and thereby give more rigor to terms like integration center, execution center, central program and locomotor memory. These terms are currently vague, but they are nonetheless useful in the quest to understand how the CNS can achieve a seamless integration of multiple motor segments for the execution of Bp locomotion.
Acknowledgments The authors express sincere appreciation to Dr. Hirotaka Onoe, Tokyo Metropolitan Institute for Neuroscience, for his help with data processing and continuous encouragement, and Dr. Carol Boliek, University of Alberta, for her critical review and editing of the original version of this manuscript. We also appreciate the technical support of Hamamatsu Photonics KK personnel, including Messrs. Takeharu Kakiuchi, Masami Futatsubashi and Dai Fukumoto. This study was supported by a Grant-in Aid for Encouragement of Young Scientists to F.M. and a Grant-in Aid for General Scientific Research to S.M. from the Ministry of Education, Science, Sports, Culture and Technology of Japan; and, a Grant in Aid on Comprehensive Research on Aging and Health to S.M. from the Ministry of Health and Welfare of Japan.
Abbreviations Bp CNS M. fuscata MTP PET Qp SPECT
bipedal central nervous system Macaca fuscata metatarsophalangeal positron emission tomography quadrupedal single photon emission computed tomography
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CHAPTER 19
Reactive and anticipatory control of posture and bipedal locomotion in a nonhuman primate Futoshi Mori1,*, Katsumi Nakajima1, Atsumichi Tachibana1, Chijiko Takasu1, Masahiro Mori1, Toru Tsujimoto2, Hideo Tsukada3 and Shigemi Mori1 1
Department of Biological Control System and 2Center for Brain Experiment, National Institute for Physiological Sciences, Okazaki 444-8585, Japan 3 PET Center, Central Research Laboratory, Hamamatsu Photonics KK, Hamakita 434-8601, Japan
Abstract: Bipedal locomotion is a common daily activity. Despite its apparent simplicity, it is a complex set of movements that requires the integrated neural control of multiple body segments. We have recently shown that the juvenile Japanese monkey, M. fuscata, can be operant-trained to walk bipedally on moving treadmill. It can control the body axis and lower limb movements when confronted by a change in treadmill speed. M. fuscata can also walk bipedally on a slanted treadmill. Furthermore, it can learn to clear an obstacle attached to the treadmill’s belt. When failing to clear the obstacle, the monkey stumbles but quickly corrects its posture and the associated movements of multiple motor segments to again resume smooth bipedal walking. These results give indication that in learning to walk bipedally, M. fuscata transforms relevant visual, vestibular, proprioceptive, and exteroceptive sensory inputs into commands that engage both anticipatory and reactive motor mechanisms. Both mechanisms are essential for meeting external demands imposed upon posture and locomotion.
Introduction
commands; an execution center for the initiation, sustenance, goal-directed modification and termination of locomotion (Mori, 1997; S. Mori et al., Chapter 33 of this volume); and, a central program, which integrates selected cognitive and emotive information and stores it as ‘locomotor memory’ (McFadyen and Be´langer, 1997). These centers appear to reside within the cerebellum, basal ganglia and cerebral cortex, and their interconnecting pathways (Brooks and Thach, 1981; Armstrong, 1986; Garcia-Rill and Skinner, 1987; Kably and Drew, 1998; Mori et al., 1999b). By integration of these lower- and higher-control mechanisms, Bp and quadrupedal (Qp) animals continuously adjust their posture and locomotion, and respond appropriately to environmental perturbations.
The elaboration of bipedal (Bp) locomotion by the human and selected nonhuman primates requires that the central nervous system (CNS) recruit and integrate lower-order automatic and higher-order volitional control mechanisms. Lower-order control is comprised of several posture- and locomotorrelated subprograms stored in the brainstem and spinal cord (Mori, 1987; S. Mori et al., Chapter 33 of this volume). Conceptually, higher-order control involves at least three major subsystems: an integration center for postural and locomotor *Corresponding author: Tel.: þ 81-564-55-7772; Fax: þ 81-564-52-7913; E-mail: [email protected]
191 DOI: 10.1016/S0079-6123(03)43019-7
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Accommodation to the external environment requires both reactive and anticipatory control mechanisms, which are presumed to reside in lower and higher parts of the CNS, respectively (Wall et al., 1981; Mori, 1987; Patla et al., 1991; Lange et al., 1996; McFadyen and Be´langer, 1997). The use of these two CNS mechanisms provides the basis for successful Bp navigation on slanted, uneven and obstacle-impeded walking surfaces, all with a seamless integration of total posture and movement of individual motor segments. For this, the CNS must take into account the ongoing state of the spinal mechanisms and locomotor apparatus, e.g., the phase of the locomotor cycle (Arshavsky et al., 1986). In addition, CNS-controlled, visuomotor coordination is apparently one of the key factors for the successful execution of unaided locomotion (Georgopoulos and Grillner, 1986; Drew, 1991; Patla et al., 1991). Inadequate incorporation of proprioceptive, exteroceptive, visual and vestibular information into the motor commands from the integration center may be one of the causes of disintegration of a number of motor segments, thereby resulting in stumbling and other unstable forms of locomotion. We have recently shown that the Japanese monkey, Macaca fuscata, is a valuable nonhuman primate Bp model for potentially advancing understanding of CNS mechanisms that contribute to the control of postural and locomotor behavior (Mori et al., 1996; Nakajima et al., 2001). This animal is normally Qp but it can be operant-trained to use Bp locomotion on the surface of a moving treadmill belt. In the latter mode, we have recently examined M. fuscata’s reactive and anticipatory motor behavior during various walking tasks. It should be mentioned here that the monkey’s Bp walking is digitigrade and it differs from the plantigrade walking of humans, which is characterized by heel-strike and toe-off (Carlso¨o¨, 1972). Nevertheless, both single and double support phase by the lower limbs were observed during execution of monkey’s Bp walking. In the following sections, we first present a kinematic analysis of the animal’s reactive capability during Bp locomotion on a slanted treadmill belt (Mori et al., 1999a). Next, we show its anticipatory and reactive capability when accommodating an obstacle on a horizontal treadmill belt (Mori et al., 2001a; see also Nakajima et al., Chapter 18 of this volume).
Reactive locomotor patterns during slanted walking Bp locomotion in humans and nonhuman primates must simultaneously meet several requirements, including: (1) antigravity support, (2) stepping movements, (3) equilibrium and (4) propulsion (Martin, 1967; Mori, 1997). The force for the latter is provided by the weight of the body ‘sliding down an incline’ with forward movement. To accommodate a constantly changing environment, the neural mechanisms for the requirements must be coordinated. For example, uphill and downhill (slanted) Bp walking by humans require specific modifications in lower-limb kinematics and the supporting body posture (Martin, 1967; Brandell, 1977; Wall et al., 1981; Kawamura et al., 1991; Lange et al., 1996; Leroux et al., 1999). In uphill versus level walking, the legs need to generate a larger acceleration force in order to transfer the center of body mass forward. In parallel, postural adjustments are also required to maintain body equilibrium and facilitate generation of forward propulsive force. In downhill walking, the legs need to generate a net deceleration force to brake forward transfer of the center of body mass. Again, postural adjustments facilitate this braking. We have examined these responses during the skilled Bp locomotion of M. fuscata with a focus on the extent to which its movements resemble those of the human. Prior to slanted walking, M. fuscata was operanttrained to use both a Qp and Bp gait while walking on a level treadmill belt at different speeds (for methods, see Mori et al., 1996; Nakajima et al., 2001). Once mastered, the animal was challenged with slanted tasks. Figure 1 shows the exemplary walking patterns of M. fuscata on uphill ( þ 15 ) and downhill (15 ) grades at a fixed treadmill speed (1.3 m/s). Superimposed on the drawings are exemplary walking patterns of the same monkey on a level grade at the same treadmill speed. Lines have been drawn on the animal sketches to depict relevant kinematic and joint angles: ear–hip angle and the angles at the hip, knee, ankle and metatarsophalangeal (MTP) joints. The line between ear and hip represents the body’s axis. Figure 1A–B show the instantaneous postural shift when the monkey placed the foot of its left,
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Fig. 1. Schematic drawings of M. fuscata during Bp level versus slanted walking at the same speed. Open drawings show body position and stride on a level (0 ) treadmill belt. Filled drawings show the same animal during uphill (A, þ 15 ) and downhill (B, 15 ) walking. In all cases, the belt speed was 1.3 m/s. In this and Fig. 2, the treadmill belt was moving from left to right, and the monkey was walking from right to left. Drawings are superimposed with reference to the hip joint. Arrows indicate the changes in body axis from level to uphill (A), and level to downhill (B) walking.
forward limb on the moving treadmill belt (i.e., touchdown; onset of the stance phase of the left limb). Next, the monkey lifted the foot of its right, rearward limb up from the surface of the treadmill belt (i.e., takeoff; onset of the swing phase of the right limb). In uphill walking (Fig. 1A), the monkey inclined its body axis maximally during the stance phase of both limbs. The extent of forward body axis inclination was much larger than that observed during level walking. Throughout a single uphill versus level step cycle, the monkey exhibited: (1) a larger flexion of the hip joint, lesser extension of the knee joint and a larger ankle dorsiflexion during the mid-swing and early stance phase; and (2) a larger knee joint extension in the late stance phase. In downhill walking (Fig. 1B), the monkey declined its body axis maximally during the stance phase of both limbs. The extent of body axis declination was much larger than that observed during level walking.
Throughout a single downhill versus level step cycle, the monkey exhibited: (1) a larger extension of the knee joint and lesser flexion of the hip joint during the late swing and early stance phase; and (2) a lesser extension of the hip joint and larger flexion of the knee joint during the late stance and early swing phase. These coordinated hip–knee flexion–extension patterns were also observed in knee–ankle joints. Figure 1 also shows that forward inclination and backward declination of the body axis increased proportionately with an increase in treadmill angle (upward or downward, respectively) and treadmill speed. An uphill increase in treadmill angle from 0 to 7 to 15 at a constant treadmill speed resulted in an increase in the maximum degree of forward inclination from 15 to 24 to 37 at a fixed treadmill speed (1.3 m/s), respectively. Similarly, a downhill increase in treadmill angle from 0 to 7 to 15 at the same treadmill speed resulted in a decrease in the maximum
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inclination degree of body axis from 15 to 8 to 2 , respectively. This relationship between changes in treadmill angle and maximum inclination/declination of the body axis was near linear across all three of the tested treadmill speeds (0.7, 1.0 and 1.3 m/s). During level treadmill walking at a fixed speed (0.7 m/s), the duration of the stance and swing phase of the step was 0.60 and 0.25 s, respectively. Uphill and downhill walking involved more prolonged and shortened stance-phase duration, respectively. This relationship was maintained across the tested treadmill speeds. The duration of the swing phase of the step did not change significantly, however. We found a linear relationship between treadmill angle and stride length, i.e., a progressively longer stride for an increase in treadmill angle from 15 to þ 15 . We also found associations between stride length, treadmill angle and treadmill speed. During uphill walking, step-cycle frequency decreased as stride length and treadmill speed was increased, the reverse occurring during downhill walking. Healthy humans make quite similar adjustments to those described for slanted walking (Wall et al., 1981; Kawamura et al., 1991; Leroux et al., 1999). Taken together, these results suggest that the operant-trained Bp locomotion of M. fuscata is smooth and versatile under varying external conditions, and its functional coupling between the lower limbs and body posture is quite similar to that of humans. The results demonstrate that for Bp walking, the monkey has acquired optimal CNS parameters for the coordination of multiple motor segments during slanted walking.
Anticipatory and reactive adjustments during obstacle-encountered treadmill walking During everyday human locomotion, the feet often collide with unexpected obstacles, thereby requiring compensatory postural and gait adjustments to prevent stumbling and falling, and reestablish smooth walking. Such adjustments have been studied experimentally in the human by having the subject walk on an obstacle-obstructed pathway (Eng et al., 1994) or a moving treadmill belt (Schillings et al., 1996). Similarly, Dietz et al. (1987) studied stumbling-corrective reactions in humans by accelerating
and decelerating the speed of a treadmill belt. These studies all demonstrated that humans use both reactive and anticipatory postural adjustments to perturbations encountered while walking (McFadyen and Be´langer, 1997). Such adjustments occur in a proactive way during all phases of the step cycle, with visuomotor coordination a critical factor for anticipatory adjustments. In order to successfully judge distances and modify step length to attain a target or avoid an obstacle, the human needs but intermittent visual sampling of the immediate environment (Georgopoulos and Grillner, 1986; Drew, 1991; Patla et al., 1991). We have tested the extent to which M. fuscata can perform similarly during its Bp locomotion. Figure 2 shows that we trained M. fuscata to step over an adjustable-height rectangular block (width: 25 cm; length: 5 cm; height: 2.4, 5.0 and 7.0 cm) that was placed on the left side of a treadmill belt. The obstacle was arranged to confront the left limb every 4–6 steps, as dependent on belt speed. In this situation, the monkey could be motivated to walk continuously for 3–5 min, with such continuity termed a single trial. In a single trial, the monkey encountered the obstacle 40–70 times. A 3–4-min rest was needed between trials to insure that the animal maintained a relatively constant level of reward-based motivation (Mori et al., 2001a). Successive trials involved use of different combinations of fixed treadmill speed (0.7–1.3 m/s) and obstacle height. During initial trials, the monkey often stumbled when the toe of the trailing left foot stepped on the obstacle’s top (horizontal) surface, or slipped up on the initially encountered (vertical) surface. After several sequential trials, the number of stumbles in a single trial was reduced, i.e., the monkey gradually learned to clear the obstacle at various walking speeds, by use of what in humans has been termed a ‘hip–knee flexion strategy’ (McFadyen and Winter, 1991). This involved the monkey increasing the extent of flexion of the trailing left limb’s hip and knee joint while simultaneously, the leading right limb alone supported the center of body mass and maintained equilibrium. When the obstacle’s height was raised, there was a corresponding increase in hip/knee joint flexion of the trailing limb so as to produce sufficient clearance space above the obstacle.
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Figure 2A shows M. fuscata’s exemplary walking pattern during the control (no-obstacle) condition. Figures 2B–D show patterns observed at different times during the perturbation (obstacle-on) condition: B, with the in-coming obstacle 3–4 steps ahead and out-of-sight; and C, a successful clearance; and D, recovery after an unsuccessful clearance. In the control (Fig. 2A) state, the center of body mass was supported by the leading (right) limb alone when the trailing left limb was at its mid-swing phase with moderate flexion at the hip and knee joints. When the in-coming obstacle was still out-of-sight (Fig. 2B), but probably anticipated, the hip and knee flexion extent of trailing limb was more pronounced. This effect was exaggerated even further during successful clearance of the obstacle (Fig. 2C), which also included a further dorsiflexion of the ankle. When the animal encountered the obstacle during the period of early- to mid-swing phase, it easily cleared the obstacle. With some presumably visual information, it could adjust the trajectory of left foot even during the late period of swing phase and successfully clear the obstacle. Figure 2 does not
show that in this latter case, the trailing limb at the swing phase undertook a longer and more prolonged stride to maintain equilibrium. During this task, there was no significant change in the body’s axis, and the head was maintained at a relatively constant position. When the trailing foot failed to clear the obstacle (Fig. 2D), stumbling occurred routinely. Such stumbling usually involved either stepping on, or slipping up, the obstacle during the late swing phase of the trailing left limb’s step. Figure 2D shows the pronounced postural perturbation associated with slipping up the obstacle. Immediately after foot– obstacle contact, the monkey slightly moved its body axis backward. This was followed immediately by a rapid and pronounced ( 40 ) forward movement of the body axis. Subsequently, the animal: (1) shortened the swing period of the leading limb; (2) flexed the left and right lower limb joints to lower the center of body mass to the treadmill belt; (3) extended its left (and/or right) forelimb forward and/or downward; and finally (4) extended its lower limb joints to raise the lowered
Fig. 2. Schematic drawings of the mid-swing phase of the left hindlimb during normal versus obstacle-encountered, level Bp walking. (A) Control (no-obstacle) walking at 1.0 m/s. (B–D) Walking at the same speed, but in the obstacle-encountered situation. (B) Obstacle 3–4 steps ahead of monkey and out-of-sight. (C) A successful clearance of the obstacle; and (D) the defensive posture that occurred after stumbling over the obstacle.
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body mass to the preperturbed position. The first three compensatory reactions of multiple motor segments served to stabilize the perturbed posture. When the animal stepped on the obstacle, it immediately initiated a new trailing limb’s swing phase from the top surface of the obstacle. In such instance, landing of the leading right foot on the treadmill belt always preceded the beginning of the trailing limb’s swing phase. Alternatively, if the trailing limb’s foot slipped up the obstacle, the animal initiated the new swing phase from the belt surface. To clear the obstacle, the monkey adjusted the trajectory of the trailing limb with the toes fully flexed. These reactive compensations for the perturbed posture finally made the animal possible to restore the position of the head, body and limb segments to preperturbed one, and to walk safely and smoothly. Recovery of walking required the restoration of (1) the center of body mass, (2) the head position and (3) the body axis to its predisturbed position in space. Interestingly, the correction of the head position always occurred first, followed by that of the body axis and upper and lower limbs. Perhaps head position in space is a critical determinant of the nature and extent of reactive responses to postural perturbations encountered during walking. From the preceding paragraphs, it can be seen that M. fuscata recruited both anticipatory and reactive control mechanisms to prepare for the incoming obstacle, even when it was still out-of-sight, and to restore the perturbed posture after stumbling over the obstacle. The latter mechanism was also used to adjust the trajectory of the trailing limb with the integration of visual information and motor output. We have also observed that the occurrence of stumbling in a single trial decreased as the monkey encountered successive obstacles. Such observations suggest that the monkey could store a novel ‘obstacle clearance strategy’ in its ‘locomotor memory’ repertoire. This was presumably acquired by motor learning.
Comment and summary Overall, the kinematic analyses of M. fuscata’s Bp locomotion indicate that this animal and the human
have similar kinematics for the integration of posture and locomotion, particularly for the hip joint. In both, hip extension proceeds from touchdown (beginning of stance phase) to takeoff (beginning of swing phase) of the foot. When the Bp-walking monkey encountered an obstacle, it changed its foot trajectory to produce a larger-than-usual successful clearance over the obstacle (hip and knee flexion strategy). Moreover when the monkey stumbled over the obstacle, it quickly recovered from its perturbed posture and movement, and continued its smooth, well-coordinated Bp walking. These findings suggest that the monkey’s CNS received and transformed salient visual, vestibular, proprioceptive and exteroceptive sensory information into output (command) motor signals appropriate for the integration of multiple body segments, this being essential for successful accommodation of the obstacle. Such a transformation process, including recall of ‘locomotor memory’, would require continual modification of the ongoing postural and locomotor control signals, which include anticipatory and reactive components. The studies described earlier show that the normally Qp M. fuscata is a valuable nonhuman primate model for studying the CNS control of not only Bp locomotion and accompanying posture, but also compensations to stumbling and falling, and eventually several other types of movement disturbance. Shibasaki’s Kyoto University group has recently used single photon emission computed tomography (SPECT) to study corridor (Fukuyama et al., 1997) and treadmill (Hanakawa et al., 1999) walking by normal adult subjects. Their results have shown a high bilateral activation in the primary sensorimotor, supplementary motor- and visual cortex, as well as in the basal ganglia and cerebellum (see also Shibasaki et al., Chapter 20 of this volume). Presumably, the CNS of the Bp-walking monkey display analogous activation patterns. To test this idea, we have recently developed a noninvasive neuroimaging protocol. Positron emission tomography (PET; Watanabe et al., 1997) is being used to measure cerebral glucose metabolism after epochs of Bp locomotion. A preliminary study has already shown that multiple brain regions are activated (Mori et al., 2001b), just as they are in humans. Some of these brain regions may reflect plastic changes in neural circuitry involved in long-term locomotor
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learning. This PET project should provide the opportunity to study experimentally how each of the activated brain regions contributes to the control of Bp posture and locomotion, including reactive and anticipatory control mechanisms. It should also contribute to further understanding of CNS circuitry required for the initiation, maintenance and recall of Bp locomotion, and thereby give more rigor to terms like integration center, execution center, central program and locomotor memory. These terms are currently vague, but they are nonetheless useful in the quest to understand how the CNS can achieve a seamless integration of multiple motor segments for the execution of Bp locomotion.
Acknowledgments The authors express sincere appreciation to Dr. Hirotaka Onoe, Tokyo Metropolitan Institute for Neuroscience, for his help with data processing and continuous encouragement, and Dr. Carol Boliek, University of Alberta, for her critical review and editing of the original version of this manuscript. We also appreciate the technical support of Hamamatsu Photonics KK personnel, including Messrs. Takeharu Kakiuchi, Masami Futatsubashi and Dai Fukumoto. This study was supported by a Grant-in Aid for Encouragement of Young Scientists to F.M. and a Grant-in Aid for General Scientific Research to S.M. from the Ministry of Education, Science, Sports, Culture and Technology of Japan; and, a Grant in Aid on Comprehensive Research on Aging and Health to S.M. from the Ministry of Health and Welfare of Japan.
Abbreviations Bp CNS M. fuscata MTP PET Qp SPECT
bipedal central nervous system Macaca fuscata metatarsophalangeal positron emission tomography quadrupedal single photon emission computed tomography
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